Activity-dependent decrease of excitability in rat hippocampal neurons through increases in Ih (original) (raw)

References

1. Bliss, T.V. & Collingridge, G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31–39 (1993).
   CAS PubMed Google Scholar
2. Andersen, P., Sundberg, S.H., Sveen, O., Swann, J.W. & Wigstrom, H. Possible mechanisms for long-lasting potentiation of synaptic transmission in hippocampal slices from guinea-pigs. J. Physiol. (Lond.) 302, 463–482 (1980).
   CAS Google Scholar
3. Bliss, T.V. & Lomo, T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. (Lond.) 232, 331–356 (1973).
   CAS Google Scholar
4. Zhang, W. & Linden, D.J. The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat. Rev. Neurosci. 4, 885–900 (2003).
   CAS PubMed Google Scholar
5. Frick, A., Magee, J. & Johnston, D. LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat. Neurosci. 7, 126–135 (2004).
   CAS PubMed Google Scholar
6. Spitzer, N.C. A developmental handshake: neuronal control of ionic currents and their control of neuronal differentiation. J. Neurobiol. 22, 659–673 (1991).
   CAS PubMed Google Scholar
7. Turrigiano, G.G. & Nelson, S.B. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 5, 97–107 (2004).
   CAS PubMed Google Scholar
8. Cudmore, R.H. & Turrigiano, G.G. Long-term potentiation of intrinsic excitability in LV visual cortical neurons. J. Neurophysiol. 92, 341–348 (2004).
   PubMed Google Scholar
9. Desai, N.S., Rutherford, L.C. & Turrigiano, G.G. Plasticity in the intrinsic excitability of cortical pyramidal neurons. Nat. Neurosci. 2, 515–520 (1999).
   CAS PubMed Google Scholar
10. Turrigiano, G., Abbott, L.F. & Marder, E. Activity-dependent changes in the intrinsic properties of cultured neurons. Science 264, 974–977 (1994).
    CAS PubMed Google Scholar
11. Aizenman, C.D. & Linden, D.J. Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons. Nat. Neurosci. 3, 109–111 (2000).
    CAS PubMed Google Scholar
12. Wang, Z., Xu, N.L., Wu, C.P., Duan, S. & Poo, M.M. Bidirectional changes in spatial dendritic integration accompanying long-term synaptic modifications. Neuron 37, 463–472 (2003).
    CAS PubMed Google Scholar
13. van Welie, I., van Hooft, J.A. & Wadman, W.J. Homeostatic scaling of neuronal excitability by synaptic modulation of somatic hyperpolarization-activated _I_h channels. Proc. Natl. Acad. Sci. USA 101, 5123–5128 (2004).
    CAS PubMed PubMed Central Google Scholar
14. Xu, J., Kang, N., Jiang, L., Nedergaard, M. & Kang, J. Activity-dependent long-term potentiation of intrinsic excitability in hippocampal CA1 pyramidal neurons. J. Neurosci. 25, 1750–1760 (2005).
    CAS PubMed PubMed Central Google Scholar
15. Daoudal, G., Hanada, Y. & Debanne, D. Bidirectional plasticity of excitatory postsynaptic potential (EPSP)-spike coupling in CA1 hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. USA 99, 14512–14517 (2002).
    CAS PubMed PubMed Central Google Scholar
16. Marder, C.P. & Buonomano, D.V. Timing and balance of inhibition enhance the effect of long-term potentiation on cell firing. J. Neurosci. 24, 8873–8884 (2004).
    CAS PubMed PubMed Central Google Scholar
17. Roberson, E.D., English, J.D. & Sweatt, J.D. A biochemist's view of long-term potentiation. Learn. Mem. 3, 1–24 (1996).
    CAS PubMed Google Scholar
18. Watanabe, S., Hoffman, D.A., Migliore, M. & Johnston, D. Dendritic K+ channels contribute to spike-timing dependent long-term potentiation in hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. USA 99, 8366–8371 (2002).
    CAS PubMed PubMed Central Google Scholar
19. Magee, J.C. & Johnston, D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275, 209–213 (1997).
    CAS PubMed Google Scholar
20. Buzsaki, G. Theta oscillations in the hippocampus. Neuron 33, 325–340 (2002).
    CAS PubMed Google Scholar
21. Thomas, M.J., Watabe, A.M., Moody, T.D., Makhinson, M. & O'Dell, T.J. Postsynaptic complex spike bursting enables the induction of LTP by theta frequency synaptic stimulation. J. Neurosci. 18, 7118–7126 (1998).
    CAS PubMed PubMed Central Google Scholar
22. Poolos, N.P., Migliore, M. & Johnston, D. Pharmacological upregulation of h-channels reduces the excitability of pyramidal neuron dendrites. Nat. Neurosci. 5, 767–774 (2002).
    CAS PubMed Google Scholar
23. Shah, M.M., Anderson, A.E., Leung, V., Lin, X. & Johnston, D. Seizure-induced plasticity of h channels in entorhinal cortical layer III pyramidal neurons. Neuron 44, 495–508 (2004).
    CAS PubMed PubMed Central Google Scholar
24. Maccaferri, G., Mangoni, M., Lazzari, A. & DiFrancesco, D. Properties of the hyperpolarization-activated current in rat hippocampal CA1 pyramidal cells. J. Neurophysiol. 69, 2129–2136 (1993).
    CAS PubMed Google Scholar
25. Shin, K.S., Rothberg, B.S. & Yellen, G. Blocker state dependence and trapping in hyperpolarization-activated cation channels: evidence for an intracellular activation gate. J. Gen. Physiol. 117, 91–101 (2001).
    CAS PubMed PubMed Central Google Scholar
26. Magee, J.C. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J. Neurosci. 18, 7613–7624 (1998).
    CAS PubMed PubMed Central Google Scholar
27. Johnston, D., Magee, J.C., Colbert, C.M. & Christie, B.R. Active properties of neuronal dendrites. Annu. Rev. Neurosci. 19, 165–186 (1996).
    CAS PubMed Google Scholar
28. Schiller, J., Schiller, Y. & Clapham, D.E. NMDA receptors amplify calcium influx into dendritic spines during associative pre- and postsynaptic activation. Nat. Neurosci. 1, 114–118 (1998).
    CAS PubMed Google Scholar
29. Mackenzie, P.J. & Murphy, T.H. High safety factor for action potential conduction along axons but not dendrites of cultured hippocampal and cortical neurons. J. Neurophysiol. 80, 2089–2101 (1998).
    CAS PubMed Google Scholar
30. Magee, J.C. & Carruth, M. Dendritic voltage-gated ion channels regulate the action potential firing mode of hippocampal CA1 pyramidal neurons. J. Neurophysiol. 82, 1895–1901 (1999).
    CAS PubMed Google Scholar
31. Robinson, R.B. & Siegelbaum, S.A. Hyperpolarization-activated cation currents: from molecules to physiological function. Annu. Rev. Physiol. 65, 453–480 (2003).
    CAS PubMed Google Scholar
32. Nolan, M.F. et al. A behavioral role for dendritic integration: HCN1 channels constrain spatial memory and plasticity at inputs to distal dendrites of CA1 pyramidal neurons. Cell 119, 719–732 (2004).
    CAS PubMed Google Scholar
33. Saar, D. & Barkai, E. Long-term modifications in intrinsic neuronal properties and rule learning in rats. Eur. J. Neurosci. 17, 2727–2734 (2003).
    PubMed Google Scholar
34. Vasilyev, D.V. & Barish, M.E. Postnatal development of the hyperpolarization-activated excitatory current _I_h in mouse hippocampal pyramidal neurons. J. Neurosci. 22, 8992–9004 (2002).
    CAS PubMed PubMed Central Google Scholar
35. Bender, R.A. et al. Differential and age-dependent expression of hyperpolarization-activated, cyclic nucleotide-gated cation channel isoforms 1–4 suggests evolving roles in the developing rat hippocampus. Neuroscience 106, 689–698 (2001).
    CAS PubMed Google Scholar
36. Zhu, J.J. Maturation of layer 5 neocortical pyramidal neurons: amplifying salient layer 1 and layer 4 inputs by Ca2+ action potentials in adult rat tuft dendrites. J. Physiol. (Lond.) 526, 571–587 (2000).
    CAS Google Scholar
37. Yuan, L.L., Adams, J.P., Swank, M., Sweatt, J.D. & Johnston, D. Protein kinase modulation of dendritic K+ channels in hippocampus involves a mitogen-activated protein kinase pathway. J. Neurosci. 22, 4860–4868 (2002).
    CAS PubMed PubMed Central Google Scholar
38. Magee, J.C. Dendritic _I_h normalizes temporal summation in hippocampal CA1 neurons. Nat. Neurosci. 2, 508 (1999).
    CAS PubMed Google Scholar
39. Berger, T., Larkum, M.E. & Luscher, H.R. High I(h) channel density in the distal apical dendrite of layer V pyramidal cells increases bidirectional attenuation of EPSPs. J. Neurophysiol. 85, 855–868 (2001).
    CAS PubMed Google Scholar
40. Berger, T. & Luscher, H.R. Associative somatodendritic interaction in layer V pyramidal neurons is not affected by the antiepileptic drug lamotrigine. Eur. J. Neurosci. 20, 1688–1693 (2004).
    PubMed Google Scholar
41. Frick, A., Magee, J., Koester, H.J., Migliore, M. & Johnston, D. Normalization of Ca2+ signals by small oblique dendrites of CA1 pyramidal neurons. J. Neurosci. 23, 3243–3250 (2003).
    CAS PubMed PubMed Central Google Scholar
42. Berridge, M.J. Neuronal calcium signaling. Neuron 21, 13–26 (1998).
    CAS PubMed Google Scholar
43. Erondu, N.E. & Kennedy, M.B. Regional distribution of type II Ca2+/calmodulin-dependent protein kinase in rat brain. J. Neurosci. 5, 3270–3277 (1985).
    CAS PubMed PubMed Central Google Scholar
44. Shen, K. & Meyer, T. Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation. Science 284, 162–166 (1999).
    CAS PubMed Google Scholar
45. Lisman, J., Schulman, H. & Cline, H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat. Rev. Neurosci. 3, 175–190 (2002).
    CAS PubMed Google Scholar
46. Santoro, B., Wainger, B.J. & Siegelbaum, S.A. Regulation of HCN channel surface expression by a novel C-terminal protein-protein interaction. J. Neurosci. 24, 10750–10762 (2004).
    CAS PubMed PubMed Central Google Scholar
47. Bi, G. & Poo, M. Synaptic modification by correlated activity: Hebb's postulate revisited. Annu. Rev. Neurosci. 24, 139–166 (2001).
    CAS PubMed Google Scholar
48. Bienenstock, E.L., Cooper, L.N. & Munro, P.W. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J. Neurosci. 2, 32–48 (1982).
    CAS PubMed PubMed Central Google Scholar
49. Ganguly, K., Kiss, L. & Poo, M. Enhancement of presynaptic neuronal excitability by correlated presynaptic and postsynaptic spiking. Nat. Neurosci. 3, 1018–1026 (2000).
    CAS PubMed Google Scholar
50. Pouille, F. & Scanziani, M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293, 1159–1163 (2001).
    CAS PubMed Google Scholar

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