Abnormal excitability of oblique dendrites implicated in early Alzheimer's: A computational study

Frontiers in Neural Circuits

Volumn 4, Issue , 2010, Pages

  Morse, Thomas M ^a   Carnevale, Nicholas T ^a   Mutalik, Pradeep G ^a   Migliore, Michele ^a,b   Shepherd, Gordon M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CNR   (Italy)

Author keywords

Action potential backpropagation; Computer model; Electrical activity

Indexed keywords

AMYLOID BETA PROTEIN; CALCIUM CHANNEL L TYPE; CALCIUM ION;

ACTION POTENTIAL; ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL INVASION; CELL MEMBRANE DEPOLARIZATION; COGNITION; DENDRITE; DENDRITIC CELL; HIPPOCAMPUS; MOUSE; NERVE FIBER; NONHUMAN; PYRAMIDAL NERVE CELL;

EID: 77953401871     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2010.00016     Document Type: Article

References (59)

1. Acker, C.D., White, J.A. (2007). Roles of IA and morphology in action potential propagation in CA1 pyramidal cell dendrites. J. Comput. Neurosci. 23:201-216.
2. Anderton, B.H., Callahan, L., Coleman, P., Davies, P., Flood, D., Jicha, G.A., Ohm, T., Weaver, C. (1998). Dendritic changes in Alzheimer's disease and factors that may underlie these changes. Prog. Neurobiol. 55:595-609
3. Andrasfalvy, B.K., Makara, J.K., Johnston, D., Magee, J.C. (2008). Altered synaptic and non- synaptic properties of CA1 pyramidal neurons in Kv4.2 knockout mice. J. Physiol. 586:3881-3892.
4. Byrne, J.H., Shepherd, G.M. (2009). Complex information processing in dendrites. In: From Molecules to Networks: An Introduction to Cellular and Molecular Neuroscience, second edition (Byrne, J. H., Roberts, J.L., ed), (San Diego: Elsevier), pp 489-512.
5. Canepari, M., Djurisic, M., Zecevic, D. (2007). Dendritic signals from rat hippocampal CA1 pyramidal neurons during coincident pre- and post-synaptic activity: a combined voltage- and calcium-imaging study. J. Physiol. 580:463-484.
6. Chen, C. (2005). beta-Amyloid increases dendritic Ca2+ influx by inhibiting the A-type K+ current in hippocampal CA1 pyramidal neurons. Biochem. Biophys. Res. Commun. 338:1913-1919.
7. Colbert, C.M., Magee, J.C., Hoffman, D.A., Johnston, D. (1997). Slow recovery from inactivation of Na+ channels underlies the activity-dependent attenuation of dendritic action potentials in hippocampal CA1 pyramidal neurons. J. Neurosci. 17:6512-6521.
8. Demont-Guignard, S., Benquet, P., Gerber, U., Wendling, F. (2009). Analysis of intracerebral EEG recordings of epileptic spikes: insights from a neural network model. IEEE Trans. on Biomed. Eng. 56(12):2782-2795.
9. Fisher, R.E., Gray, R., Johnston, D. (1990). Properties and distribution of single voltage-gated calcium channels in adult hippocampal neurons. J. Neurophysiol. 64(1):91-104.
10. Frick, A., Magee, J., Koester, H.J., Migliore, M., Johnston, D. (2003). Normalization of Ca2+ signals by small oblique dendrites of CA1 pyramidal neurons. J. Neurosci. 23:3243-3250.
11. Gasparini, S., Losonczy, A., Chen, X., Johnston, D., Magee, J.C. (2007). Associative pairing enhances action potential back-propagation in radial oblique branches of CA1 pyramidal neurons. J. Physiol. 580:787-800.
12. Golding, N.L., Kath, W.L., Spruston, N. (2001). Dichotomy of action-potential backpropagation in CA1 pyramidal neuron dendrites. J. Neurophysiol. 86:2998-3010.
13. Golding, N.L., Mickus, T.J., Katz, Y., Kath, W.L., Spruston, N. (2005). Factors mediating powerful voltage attenuation along CA1 pyramidal neuron dendrites. J. Physiol. 568:69- 82.
14. Golomb, D., Yue, C., Yaari, Y. (2006). Contribution of persistent Na+ current and M-type K+ current to somatic bursting in CA1 pyramidal cells: combined experimental and modeling study. J. Neurophysiol. 96:1912-1926.
15. Good, T.A., Murphy, R.M. (1996). Effect of beta-amyloid block of the fast-inactivating K+ channel on intracellular Ca2+ and excitability in a modeled neuron. Proc. Natl. Acad. Sci. U.S.A. 93:15130-15135.
16. Gulledge, A.T., Kampa, B.M., Stuart, G.J. (2005). Synaptic integration in dendritic trees. J. Neurobiol. 64:75-90.
17. Helmchen, F., Imoto, K., Sakmann, B. (1996). Ca2+ buffering and action-potential evoked Ca2+ 19 signaling in dendrites of pyramidal neurons. Biophys. J. 70:1069-1081.
18. Hemond, P., Epstein, D., Boley, A., Migliore, M., Ascoli, G.A., Jaffe, D.B. (2008). Distinct classes of pyramidal cells exhibit mutually exclusive firing patterns in hippocampal area CA3b. Hippocampus. 18(4):411-24.
19. Hines, M.L., Carnevale, N.T. (1997). The Neuron simulation environment. Neural. Comput. 9:1179-1209.
20. Hines, M.L., Morse, T.M., Carnevale, N.T. (2007). Model structure analysis in NEURON:Toward interoperability among neural simulators. Methods Mol. Biol. 401:91-102.
21. 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.
22. Jaffe, D.B., Ross, W.N., Lisman, J.E., Lasser-Ross, N., Miyakawa, H., Johnston, D. (1994). A model for dendritic Ca2+ accumulation in hippocampal pyramidal neurons based on fluorescence imaging measurements. J. Neurophysiol. 71(3):1065-77.
23. Jarsky, T., Roxin, A., Kath, W.L., Spruston, N. (2005). Conditional dendritic spike propagation following distal synaptic activation of hipocampal CA1 pyramidal neurons. Nature Neurosci. 8: 1667-1676.
24. Jhamandas, J.H., Cho, C., Jassar, B., Harris, K., MacTavish, D., Easaw, J. (2001). Cellular mechanisms for amyloid beta-protein activation of rat cholinergic basal forebrain neurons. J. Neurophysiol. 86:1312-1320.
25. Johnston, D., Hoffman, D.A., Colbert, C.M., Magee, J.C. (1999). Regulation of back- propagating action potentials in hippocampal neurons. Curr. Opin. Neurobiol. 9:288-292.
26. Jung, S.C., Kim, J., Hoffman, D.A. (2008). Rapid, bidirectional remodeling of synaptic NMDA receptor subunit composition by A-type K+ channel activity in hippocampal CA1 pyramidal neurons. Neuron 60:657-671.
27. Kamondi, A., Acsady, L., Buzsaki, G. (1998). Dendritic spikes are enhanced by cooperative network activity in the intact hippocampus. J. Neurosci. 18:3919-3928.
28. Katz, Y., Menon, V., Nicholson, D.A., Geinisman, Y., Kath, W.L., Spruston, N. (2009). Synapse distribution suggests a two-stage model of dendritic integration in CA1 pyramidal neurons. Neuron 63: 171-177
29. Khachaturian, Z.S. (1987). Hypothesis on the regulation of cytosol calcium concentration and the aging brain. Neurobiol. Aging 8(4):345-6.
30. Kim, J., Wei, D.S., Hoffman, D.A. (2005). Kv4 potassium channel subunits control action potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurones. J. Physiol. 569:41-57.
31. Larkum, M.E., Nevian, T., Sandler, M., Polsky, A., Schiller, J. (2009) Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: A new unifying principle. Science 325:756-760.
32. Liao, C.W., Lien, C.C. (2009). Estimating intracellular Ca2+ concentrations and buffering in a dendritic inhibitory hippocampal interneuron. Neuroscience 164:1701-1711.
33. London, M., Meunier, C., Segev, I. (1999). Signal transfer in passive dendrites with nonuniform membrane conductance. J. Neurosci. 19:8219-8233.
34. Losonczy, A., Makara, J.K., Magee, J.C. (2008). Compartmentalized dendritic plasticity and input feature storage in neurons. Nature 452:436-441.
35. Lue, L.F., Kuo, Y.M., Roher, A.E., Brachova, L., Shen, Y., Sue, L., Beach, T., Kurth, J.H., Rydel, R.E., Rogers, J. (1999). Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am. J. Pathol. 155:853-862.
36. Magee, J.C., Cook, E.P. (2000). Somatic EPSP amplitude is independent of synapse location in 20 hippocampal pyramidal neurons. Nat. Neurosci. 3:895-903.
37. Maravall, M., Mainen, Z.F., Sabatini, B.L., Svoboda, K. (2000). Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophys. J. 78:2655-2667.
38. Metz, A.E., Jarsky, T., Martina, M., Spruston, N. (2005) R-type calcium channels contribute to afterdepolarization and bursting in hippocampal CA1 pyramidal neurons. J. Neurosci. 25(24):5763-73.
39. Mickus, T., Jung, H., Spruston, N. (1999). Properties of slow, cumulative sodium channel inactivation in rat hippocampal CA1 pyramidal neurons. Biophys. J. 76:846-860.
40. Migliore, M., Ferrante, M., Ascoli, G.A. (2005). Signal propagation in oblique dendrites of CA1 pyramidal cells. J. Neurophysiol. 94:4145-4155.
41. Migliore, M., Hoffman, D.A., Magee, J.C., Johnston, D. (1999). Role of an A-type K+ conductance in the back-propagation of action potentials in the dendrites of hippocampal pyramidal neurons. J. Comput. Neurosci. 7:5-15.
42. Oh, M.M., Oliveira, F.A., Disterhoft, J.F. (2010). Learning and aging related changes in intrinsic neuronal excitability. Frontiers in Aging Neuroscience 2(2):1-10.
43. Omori, T., Aonishi, T., Miyakawa, H., Inoue, M., Okada, M. (2006). Estimated distribution of specific membrane resistance in hippocampal CA1 pyramidal neuron. Brain Res. 1125:199-208.
44. Omori T, Aonishi, T., Miyakawa H, Inoue M, Okada M (2009). Steep decrease in the specific membrane resistance in the apical dendrites of hippocampal CA1 pyramidal neurons. Neurosci. Res. 64:83-95.
45. Scheibel, A.B. (1979). The hippocampus: organizational patterns in health and senescence. Mech. Ageing Dev. 9:89-102.
46. Sjostrom, P.J., Rancz, E.A., Roth, A., Hausser, M. (2008). Dendritic excitability and synaptic plasticity. Physiol. Rev. 88:769-840.
47. Song, D., Wang, Z., Berger, T.W. (2002). Contribution of T-type VDCC to TEA-induced long- term synaptic modification in hippocampal CA1 and dentate gyrus. Hippocampus 12(5):689-97.
48. Spruston, N., Schiller, Y., Stuart, G., Sakmann, B. (1995). Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 268:297-300.
49. Stuart, G.J., Spruston, N., Häusser, M. (eds.) (2008). Dendrites: Oxford University Press.
50. Stutzmann, G.E. (2007). The pathogenesis of Alzheimers disease is it a lifelong calciumopathy? Neuroscientist 13(5):546-59.
51. Ueda, K., Shinohara, S., Yagami, T., Asakura, K., Kawasaki, K. (1997). Amyloid beta protein potentiates Ca2+ influx through L-type voltage-sensitive Ca2+ channels: a possible involvement of free radicals. J. Neurochem. 68:265-271.
52. Urakubo, H., Aihara, T., Kuroda, S., Watanabe, M., Kondo, S. (2004). Spatial localization of synapses required for supralinear summation of action potentials and EPSPs. J. Comput. Neurosci. 16:251-265.
53. Varga, A.W., Anderson, A.E., Adams, J.P., Vogel, H., Sweatt, J.D. (2000). Input-specific immunolocalization of differentially phosphorylated Kv4.2 in the mouse brain. Learn. Mem. 7:321-332.
54. Wang, J., Ikonen, S., Gurevicius, K., van Groen, T., Tanila, H. (2003). Altered auditory-evoked potentials in mice carrying mutated human amyloid precursor protein and presenilin-1 transgenes. Neuroscience 116: 511-517.
55. Watanabe, S., Hoffman, D.A., Migliore, M., Johnston, D. (2002). Dendritic K+ channels 21 contribute to spike-timing dependent long-term potentiation in hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. U.S.A. 99:8366-8371.
56. Xu, C., Qian, C., Zhang, Z., Wu, C., Zhou, P., Liang, X. (1998). Effects of beta-amyloid peptide on transient outward potassium current of acutely dissociated hippocampal neurons in CA1 sector in rats. Chin. Med. J. (Engl.) 111:492-495.
57. Ye, C.P., Selkoe, D.J., Hartley, D.M. (2003). Protofibrils of amyloid beta-protein inhibit specific K+ currents in neocortical cultures. Neurobiol. Dis. 13:177-190.
58. Yue, C., Yaari, Y. (2004). KCNQ/M channels control spike afterdepolarization and burst generation in hippocampal neurons. J. Neurosci. 24:4614-4624.
59. Zhang, C.F., Yang, P. (2006). Zinc-induced aggregation of Abeta (10-21) potentiates its action on voltage-gated potassium channel. Biochem. Biophys. Res. Commun. 345:43-49.