Locally balanced dendritic integration by short-term synaptic plasticity and active dendritic conductances

Journal of Neurophysiology

Volumn 102, Issue 6, 2009, Pages 3234-3250

  Volman, Vladislav ^a,b   Levine, Herbert ^a   Ben Jacob, Eshel ^a,c   Sejnowski, Terrence J ^a,b,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c TEL AVIV UNIVERSITY   (Israel)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; POTASSIUM ION; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL EXPERIMENT; ARTICLE; CALCIUM BINDING; CALCIUM TRANSPORT; CONTROLLED STUDY; DENDRITIC CELL; HIPPOCAMPUS; HIPPOCAMPUS THETA RHYTHM; MATHEMATICAL COMPUTING; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVE EXCITABILITY; NONHUMAN; POTASSIUM TRANSPORT; PRESYNAPTIC NERVE; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC INHIBITION;

ACTION POTENTIALS; ANIMALS; BIOPHYSICS; CA1 REGION, HIPPOCAMPAL; CALCIUM; CALCIUM CHANNELS; COMPUTER SIMULATION; DENDRITES; ELECTRIC STIMULATION; MODELS, NEUROLOGICAL; NEURAL CONDUCTION; NEURONAL PLASTICITY; PROBABILITY; PYRAMIDAL CELLS; SYNAPSES;

EID: 72749083374     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00260.2009     Document Type: Article

References (67)

1. Abbott LF, Varela JA, Sen K, Nelson SB. Synaptic depression and cortical gain control. Science 275: 221-224, 1997.
2. Andersen P, Morris R, Amaral D, Bliss T, O'Keefe J. The Hippocampus Book. New York: Oxford, 2007.
3. + conductance. Brain Res 698: 193-203, 1995.
4. Bekkers JM. Distribution of slow AHP channels on hippocampal CA1 pyramidal neurons. J Neurophysiol 83: 1756-1759, 2000. (Pubitemid 30159596)
5. Bertram R, Sherman A, Stanley EF. Single-domain/bound calcium hypothesis of transmitter release and facilitation. J Neurophysiol 75: 1919-1931, 1996.
6. Buzsaki G. Theta oscillations in the hippocampus. Neuron 33: 325-340, 2002.
7. Csicsvari J, Hirase H, Czurko A, Mamiya A, Buzsaki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 19: 274-287, 1999. (Pubitemid 29028968)
8. de la Rocha N, Parga N. Short-term synaptic depression causes a nonmonotonic response to correlated stimuli. J Neurosci 25: 8416-8431, 2005. (Pubitemid 41327382)
9. Dobrunz LE, Huang EP, Stevens CF. Very short-term plasticity in hippocampal synapses. Proc Natl Acad Sci USA 94: 14843-14847, 1997.
10. Dobrunz LE, Stevens CF. Heterogeneity of release probability, facilitation and depletion at central synapses. Neuron 18: 995-1008, 1997.
11. Eichenbaum H, Dudchenko P, Wood E, Shapiro M, Tanila H. The hippocampus, memory, and place cells: is it spatial memory or a memory space? Neuron 23: 209-226, 1999. (Pubitemid 29315717)
12. Fenton AA, Muller RU. Place cell discharge is extremely variable during individual passes of the rat through the firing field. Proc Natl Acad Sci USA 95: 3182-3187, 1998.
13. Gabbiani F, Koch C. Principles of spike train analysis. In: Methods in Neuronal Modeling, edited by Koch C, Segev I. Cambridge, MA: MIT Press, 1998, p. 313-360.
14. Garcia-Perez E, Wesseling JF. Augmentation controls the fast rebound from depression at excitatory hippocampal synapses. J Neurophysiol 99: 1770-1786, 2008. (Pubitemid 351550072)
15. Gasparini S, Magee JC. State-dependent dendritic computation in hippocampal CA1 pyramidal neurons. J Neurosci 26: 2088-2100, 2006. (Pubitemid 43295860)
16. Golding NL, Kath WL, Spruston N. Dichotomy of action-potential backpropagation in CA1 pyramidal neuron dendrites. J Neurophysiol 86: 2998-3010, 2001. (Pubitemid 33139067)
17. Harris KM, Jensen FE, Tsao B. 3D structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci 12: 2685-2705, 1992.
18. Hines ML, Carnevale NT. NEURON: a tool for neuroscientist. Neuroscientist 7: 123-135, 2001.
19. Hoffman DA, Magee JC, Colbert CM, Johnston D. K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387: 869-875, 1997. (Pubitemid 27289580)
20. Holt GR, Softky WR, Koch C, Douglas RJ. Comparison of discharge variability in-vitro and in-vivo in cat visual cortex neurons. J Neurophysiol 75: 1806-1814, 1996.
21. Ishizuka N, Cowan WM, Amaral DG. A quantitative analysis of the dendritic organization of pyramidal cells in the rat hippocampus. J Comp Neurol 362: 17-45, 1995.
22. Klyachko VA, Stevens CF. Excitatory and feed-forward inhibitory hippocampal synapses work synergistically as an adaptive filter of natural spike trains. PLoS Biol 4: e207, 2006.
23. Larkum ME, Nevian T. Synaptic clustering by dendritic signalling mechanisms. Curr Opin Neurobiol 18: 321-331, 2008.
24. Le Ray D, de Sevilla DF, Porto AB, Fuenzalida M, Buno W. Heterosynaptic metaplastic regulation of synaptic efficacy in CA1 pyramidal neurons of rat hippocampus. Hippocampus 14: 1011-1025, 2004. (Pubitemid 40073661)
25. Li X, Ascoli GA. Computational simulation of the input-output relationship in hippocampal pyramidal cells. J Comput Neurosci 21: 191-209, 2006. (Pubitemid 44237461)
26. Liu G. Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites. Nat Neurosci 7: 373-379, 2004. (Pubitemid 38429177)
27. Lorincz A, Notomi T, Tamas G, Shigemoto R, Nusser Z. Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat Neurosci 5: 1185-1193, 2002. (Pubitemid 35247178)
28. Magee JC. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18: 7613-7624, 1998. (Pubitemid 28441004)
29. 2+ influx in the dendrites of hippocampal pyramidal neurons. J Neurophysiol 74: 1335-1342, 1995.
30. Magee JC, Cook EP. Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nat Neurosci 3: 895-903, 2000.
31. 2+ channels in apical dendrites of rat CA1 pyramidal neurons. J Physiol 487: 67-90, 1995.
32. Mainen ZF, Sejnowski TJ. Modeling active dendritic processes in pyramidal neurons. In: Methods in Neuronal Modeling, edited by Koch C, Segev I. Cambridge, MA: MIT Press, 1998, p. 171-209.
33. Maletic-Savatic M, Malinow R, Svoboda K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283: 1923-1927, 1999.
34. Migliore M, Ferrante M, Ascoli GA. Signal propagation in oblique dendrites of CA1 pyramidal neurons. J Neurophysiol 94: 4145-4155, 2005. (Pubitemid 41691775)
35. + conductance in back-propagation of action potentials in the dendrites of hippocampal pyramidal neurons. J Comput Neurosci 7: 5-15, 1999.
36. Migliore M, Shepherd GM. Emerging rules for the distributions of active dendritic conductances. Nat Rev Neurosci 3: 362-370, 2002. (Pubitemid 135706633)
37. Muller RU, Kubie JL, Ranck JB. Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J Neurosci 7: 1935-1950, 1987.
38. Murthy VN, Sejnowski TJ, Stevens CF. Dynamics of dendritic calcium transients evoked by quantal release at excitatory hippocampal synapses. Proc Natl Acad Sci USA 97: 901-906, 2000.
39. Nadkarni S, Jung P. Modeling synaptic transmission of the tripartite synapse. Phys Biol 4: 1-9, 2007. (Pubitemid 46553672)
40. O'Keefe J, Nadel L. The Hippocampus as a Cognitive Map. Oxford, UK: Clarendon Press, 1978.
41. Olypher AV, Lansky P, Fenton AA. Properties of the extra-positional signal in hippocampal place cell discharge derived from the over-dispersion in location-specific firing. Neuroscience 111: 553-566, 2002. (Pubitemid 34525098)
42. 2+-dependent AHPs and firing behavior in neocortical pyramidal neurons. J Neurophysiol 79: 2522-2534, 1998.
43. Poirazi P, Brannon TM, Mel BW. Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell. Neuron 37: 977-987, 2003a. (Pubitemid 36398302)
44. Poirazi P, Brannon TM, Mel BW. Pyramidal neuron as two-layer neural network. Neuron 37: 989-999, 2003b. (Pubitemid 36398303)
45. Poolos NP, Migliore M, Johnston D. Pharmacological up-regulation of H-channels reduces the excitability of pyramidal neuron dendrites. Nat Neurosci 5: 767-774, 2002. (Pubitemid 34827595)
46. Prescott SA, Sejnowski TJ. Spike-rate coding and spike-time coding are affected oppositely by different adaptation mechanisms. J Neurosci 28: 13649-13661, 2008.
47. Reyes AD. Influence of dendritic conductances on the input-output properties of neurons. Annu Rev Neurosci 24: 653-675, 2001. (Pubitemid 32695242)
48. Sah P, Bekkers JM. Apical dendritic location of slow afterhyperpolarization current in hippocampal pyramidal neurons: implications for the integration of long-term potentiation. J Neurosci 16: 4537-4542, 1996. (Pubitemid 26251050)
49. i reveals slow kinetics of potassium channels underlying the afterhyperpolarization in hippocampal pyramidal neurons. J Neurosci 19: 3657-3664, 1999.
50. Salinas E, Sejnowski TJ. Impact of correlated synaptic input on output firing rate and variability in simple neuronal models. J Neurosci 20: 6193-6209, 2000. (Pubitemid 30658413)
51. 2+- dependent conductances in rat neocortical pyramidal neurons. J Neurophysiol 78: 187-198, 1997.
52. Shadlen MN, Newsome WT. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci 18: 3870-3896, 1998.
53. Shah MM, Haylett DG. Calcium channels involved in the generation of the slow afterhyperpolarization in cultured rat hippocampal pyramidal neurons. J Neurophysiol 83: 2554-2561, 2000.
54. Softky WR. Simple codes versus efficient codes. Curr Opin Neurobiol 5: 239-247, 1995.
55. Softky WR, Koch C. The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13: 334-350, 1993. (Pubitemid 23028748)
56. Stemmler M, Koch C. How voltage-dependent conductances can adapt to maximize the information encoded by neuronal firing rate. Nat Neurosci 2: 521-527, 1999. (Pubitemid 30491232)
57. Stevens CF, Tsujimoto T. Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool. Proc Natl Acad Sci USA 92: 846-849, 1995.
58. Stuart G, Spruston N, Hausser MH. Dendrites. Oxford, UK: Oxford University Press, 1999.
59. Tombaugh GC, Rowe WB, Rose GM. The slow afterhyperpolarization in hippocampal CA1 neurons covaries with spatial learning ability in aged Fisher 344 rats. J Neurosci 25: 2609-2616, 2005.
60. + conductance or by blocking BK channels. J Neurophysiol 89: 909-921, 2003.
61. Troyer TW, Miller KD. Physiological gain leads to high ISI variability in a simple model of a cortical regular spiking cell. Neural Comput 9: 971-983, 1997.
62. 2+ channels at the base of major dendrites in hippocampal pyramidal neurons. Nature 347: 281-284, 1990.
63. Williams SR, Stuart GJ. Role of dendritic synapse location in the control of action potential output. Trends Neurosci 26: 147-152, 2003.
64. Wilson CJ, Kawaguchi Y. The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci 16: 2397-2410, 1996. (Pubitemid 26154349)
65. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. J Neurophysiol 27: 623-633, 2000. (Pubitemid 30951862)
66. Yuste R, Denk W. Dendritic spines as basic units of synaptic integration. Nature 375: 682-684, 1995.
67. Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405, 2002.