Information processing in the axon

Nature Reviews Neuroscience

Volumn 5, Issue 4, 2004, Pages 304-316

  Debanne, Dominique ^a  

^a INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM CHANNEL; SODIUM CHANNEL;

ACTION POTENTIAL; BRAIN ELECTROPHYSIOLOGY; BRAIN REGION; CORTICAL SYNCHRONIZATION; DENDRITE; GEOMETRY; INFORMATION PROCESSING; NERVE CONDUCTION; NERVE FIBER; NEUROTRANSMISSION; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; REVIEW; SPIKE;

EID: 1842782507     PISSN: 1471003X     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrn1397     Document Type: Review

References (145)

1. Ramón y Cajal, S. Histologie du Système Nerveux (Maloine, Paris, 1911)
2. Huxley, A. From overshoot to voltage clamp. Trends Neurosci. 25, 553-558 (2002).
3. Poliak, S. & Peles, E. The local differentiation of myelinated axons at nodes of ranvier. Nature Rev. Neurosci. 4, 968-980 (2003).
4. Bostock, H., Sherrat, R. M. & Sears, T. A. Overcoming conduction failure in demyelinated nerve fibres by proloning action potentials. Nature 274, 385-387 (1978).
5. Bostock, H., Sears, T. A. & Sherratt, R. M. The effects of 4-aminopyridine and tetraethylammonium ions on normal and demyelinated mammalian nerve fibres. J. Physiol. (Lond.) 313, 301-315 (1981).
6. + channel protein in rat central neurons. Neuron 9, 243-259 (1992).
7. + channels detercted in vivo. Nature 365, 72-75 (1993).
8. + channels in terminals and juxtaparanodal regions of neurons. Nature 365, 75-79 (1993).
9. v1.2, two K channel proteins, to synaptic terminals, somata, and dendrites in the mouse brain. J. Neurosci. 14, 4588-4599 (1994).
10. v1 channel subunits: contrasting subcellular locations and neuron-specific co-localizations in rat brain. Eur. J. Neurosci. 7, 2189-2205 (1995)
11. v1.4-containing A-type potassium channels near excitatory synapses in the hippocampus. J. Neurosci. 18, 965-974 (1998).
12. v3.1b is an novel component of CNS nodes. J. Neurosci. 23, 4509-4518 (2003).
13. v1.2 channels suppress synaptic terminal hyperexcitability following action potential invasion. J. Physiol. (Lond.) 550, 27-33 (2003).
14. v3 potassium channels at the Calyx of Field presynaptic terminal. J. Neurosci. 23, 10445-10453 (2003).
15. Jonas, P., Koh, D. S., Kampe, K., Hermsteiner, M. & Vogel, W. ATP-sensitive and Ca-activated K channels in vertebrate as novel links between metabolism and excitability. Pflugers Arch. 418, 68-73 (1991).
16. + channels in rat brain: targeting to axons and nerve terminals. J. Neurosci. 16, 955-963 (1996).
17. Bielefeldt, K. & Jackson, M. B. A calcium-activated potassium channel causes frequency-dependent action-potential failures in a mammalian nerve terminal. J. Neurophysiol. 70, 284-298 (1993).
18. + channels in glutamatergic hippocampal terminals and their role in spike repolarization and regulation of transmitter release. J. Neurosci. 21, 9585-9597 (2001).
19. Roncarati, R., Di Chio, M., Save, A., Terstappen, G. C. & Fumagalli, G. Presynaptic localization of the small conductance calcium-activated potassium channel SK3 at the neuromuscular junction. Neuroscience 104, 253-262 (2001).
20. + channels localized in the nodal region of myelinated axons of Xenopus. J. Physiol. (Lond.) 479, 183-197 (1994)
21. Bhattacharjee, A., Gan, L. & Kaczmarek, L. K. Localization of the Slack potassium channel in the rat central nervous system. J. Comp. Neurol. 454, 241-254 (2002).
22. Baker, M., Bostock, P., Grafe, P. & Martins, P. Function and distribution of three types of rectifying channel in rat spinal root myelinated axons. J. Physiol. (Lond.) 383, 45-87 (1987).
23. Angstadt, J. D. & Calabrese, R. L. A hyperpolarization-activated inward current in heart interneurons of the medicinal leech. J. Neurosci. 9, 2846-2857 (1989).
24. Eng, D. L., Gordon, T. R., Kocsis, J. D. & Waxman, S. G. Current-clamp analysis of a time-dependent rectification in rat optic nerve. J. Physiol. (Lond.) 421, 185-202 (1990).
25. h channels. Nature Neurosci. 3, 133-141 (2000).
26. h activation and actin: involvement in long-term facilitation and cAMP-induced synaptic enhancement. Neuron, 33, 601-613 (2002).
27. Southan, A. P., Morris, N. P., Stephens, G. J. & Robertson, B. Hyperpoladzation-activated currents in presynaptic terminals of mouse cerebellar bascket cells. J. Physiol. (Lond.) 526, 91-97 (2000).
28. n) at an excitatory synaptic terminal in the rat auditory brainstem. J. Physiol. (Lond.) 534, 733-744 (2001).
29. Strübing, C., Krapivinsky, G., Krapivinsky, L. & Clapham, D. E. TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 29, 645-655 (2001).
30. Greka, A., Navarro, B., Oancea, E., Duggan, A. & Clapham, D. E. TRPC5 is a regulator of hippocampal neurite length and growth cone morphology. Nature Neurosci. 6, 837-845 (2003).
31. + channels in hippocampal mossy fiber boutons. Neuron 28, 927-939 (2000). With elegant recording techniques this paper shows that repetitive axon stimulation inactivates A-type potassium channels, broadens presynaptic action potentials and facilitates synaptic transmission.
32. + channel complexes. J. Neurosci. 17, 8246-8258 (1997).
33. Grossman, Y., Parnas, I. & Spira, M. E. Differential conduction block in branches of a bifurcating axon. J. Physiol. (Lond.) 295, 283-305 (1979). Demonstration and analysis of differential propagation block at the branch point of a lobster peripheral axon.
34. Wang, L. Y. & Kaczmarek, L. K. High-frequency firing help replenish the readily releasable pool of synaptic vesicles. Nature 394, 384-388 (1998).
35. Madeja, M. Do neurons have a reserve of sodium channels for the generation of action potentials? A study on acutely isolated CA1 neurons from the guinea-pig hippocampus. Eur. J. Neurosci. 12, 1-7 (2000).
36. Brody, D. L. & Yue, D. T. Release-independent short-term synaptic depression in cultured hippocampal neurons. J. Neurosci. 20, 2480-2494 (2000). Evidence that sodium channel inactivation might participate in short-term synaptic depression at autaptic contacts.
37. Prakriya, M. & Mennerick, S. Selective depression of low-release probability excitatory synapses by sodium channel blockers. Neuron 26, 671-682 (2000). Differential sensitivity of glutamatergic and GABA-mediated axons to low concentrations of sodium channel blockers.
38. + channel inactivation to paired-pulse synaptic depression in cultured hippocampal neurons. J. Neurophysiol. 87, 925-936 (2002).
39. Meeks, J. P. & Mennerick, S. The selective effects of potassium elevation on glutamate signaling and action potential conduction in hippocampus. J. Neurosci. 24, 197-206 (2004).
40. + channel gating between fast-spiking interneurones and principal neurons of rat hippocampus. J. Physiol. (Lond.) 505, 593-603 (1997).
41. Martina, M., Vida, I. & Jonas, P. Distal initiation and active propagation of action potentials in interneurons dendrites. Science 287, 295-300 (2000).
42. 2+ signals and calcium channels in axons of developing rat cerebellar interneurones. J. Physiol. (Lond.) 527, 33-48 (2000).
43. 2+ concentration rises in rat cerebellar basket cell axons. J. Physiol. (Lond.) 520, 65-78 (2000).
44. Antonini, A., Gillespie, D. C., Crair, M. C. & Stryker, M. P. Morphology of single geniculocortical afferents and functional recovery of the visual cortex after reverse monocular deprivation in the kitten. J. Neurosci. 18, 9896-9909 (1998).
45. Petersen, C., Grinvald, A. & Sakmann, B. Spatiotemporal dynamics of sensory responses in layer 2/3 of rat barrel cortex measured in vivo by voltage-sensitive dye imaging combined with whole-cell voltage recordings and neuron reconstructions. J. Neurosci. 23, 1298-1309 (2003).
46. Ishizuka, N., Weber, J. & Amaral, D. G. Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J. Comp. Neurol., 295, 580-623 (1990).
47. Major, G., Larkman, A. U., Jonas, P., Sakmann, B. & Jack, J. J. B. Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices. J. Neurosci. 14, 4613-4638 (1994).
48. Li, X., Somogyi, P., Ylinen, A. & Buzsaki, G. The hippocampal CA3 network: an in vivo intracellular labeling study. J. Comp. Neurol. 339, 181-208 (1994).
49. Gulyas, A. I., Miles, R., Hajos, N. & Freund, T. Precision and variability in postsynaptic target selection of inhibitory cells in the hippocampus CA3 region. Eur. J. Neurosci. 5, 1729-1751 (1993).
50. Guillery, R. W. Branching thalamic afferents link action and perception. J. Neurophysiol. 90, 539-548 (2003).
51. Pinault, D. & Deschênes, M. Projection and innervation patterns of individual thalamic reticular axons in the thalamus of the adult rat: a three-dimensional, graphic, and morphometric analysis. J. Comp. Neurol. 391, 180-203 (1998).
52. Westrum, L. E. & Blackstad, T. W. An electron microscopic study of the stratum radiatum of the rat hippocampus (regio superior, CA1) with particular emphasis on synaptology. J. Comp. Neurol. 119, 281-309 (1962).
53. Shepherd, G. M. G., Raastad, M. & Andersen, P. General and variable features of varicosity spacing along unmyelinated axons in the hippocampus and cerebellum. Proc. Natl Acad. Sci. USA 99, 6340-6345 (2002).
54. Blackstad, T. W. & Kjaerheim, Å. Special axo-dendritic synapses in the hippocampal cortex: electron and light microscopic studies in the hippocampal cortex: electron and light microscopic studies on the layer of mossy fibers. J. Comp. Neurol. 117, 133-146 (1961).
55. Shepherd, G. M. G. & Raastad, M. Axonal varicosity ditributins along parallel fibers: a new angle on a cerebellar circuit. Cerebellum 2, 110-113 (2003).
56. Young, J. Z. The giant nerve fibres and epistellar body of cephalopods. Q. J. Microsc. Sci. 78, 367-386 (1936).
57. Berbel, P. & Innocenti, G. M. The development of the corpus callosum: a light and electromicroscopic study. J. Comp. Neurol. 276, 132-156 (1988).
58. Chung, S. H., Raymond, S. A. & Lettvin, J. Y. Multiple meaning in single visual units. Brain Behav. Evol. 3, 72-101 (1970).
59. Carr, C. E. & Konishi, M. Axonal delay lines for time measurement in the owl's brainstem. Proc. Natl Acad. Sci. USA 85, 8311-8315 (1988).
60. Carr, C. E. & Konishi, M. A circuit for detection of interaural time differences in the brain stem of the barn owl. J. Neurosci. 10, 3227-3246 (1990).
61. McAlpine, D. & Grothe, B. Sound localization and delay lines - do mammals fit the model? Trends Neurosci. 26, 347-350 (2003).
62. Manor, Y., Koch, C. & Segev, I. Effect of geometrical irregularities on propagation delay in axonal trees. Biophys. J. 60, 1424-1437 (1991). A theoretical study showing how the numerous branch points introduce a delay of conduction in axon collaterals.
63. Lüscher, C., Streit, J. Quadroni, R. & Lüscher, H. R. Action potential propagation through embryonic dorsal root ganglion cells in culture. I. Influence of the cell morphology on propagation properties. J. Neurophysiol. 72, 622-633 (1994).
64. Hatt, H. & Smith, D. O. Synaptic depression related to presynaptic axon conduction block. J. Physiol. (Lond.) 259, 367-393 (1976).
65. Streit, J., Lüscher, C. & Lüscher, H. R. Depression of postsynaptic potentials by high frequency stimulation in embryonic motoneurons grown in spinal cord slice cultures. J. Neurophysiol. 68, 1793-1803 (1992).
66. + conductance in hippocampus. Nature 389 286-289 (1997). Failures of transmission interpreted as propagation failures are observed in hippocampal neurons when the presynaptic action potential is evoked following a transient somatic hyperpolarization.
67. Muschol, M., Kosterin, P., Ichikawa, M. & Salzberg, B. M. Activity-dependent depression of excitability and calcium transients in the neurohypophysis suggests a model of 'stuttering conduction'. J. Neurosci. 23, 11352-11362 (2003).
68. Barron, D. H. & Matthews, B. H. C. Intermittent conduction in the spinal cord. J. Physiol. (Lond.) 85, 73-103 (1939).
69. Krnjevic, K. & Miledi, R. Presynaptic failure of neuromuscular propagation in rats. J. Physiol. (Lond.) 149, 1-22 (1959).
70. Pamas, I. Differential block at high frequency of branches of a single axon innervating two muscles. J. Neurophysiol. 35, 903-914 (1972).
71. Smith, D. O. Mechanisms of action potential propagation failure at sites of axon branching in the crayfish. J. Physiol. (Lond.) 301, 243-259 (1980).
72. Van Essen, D. C. The contribution of membrane hyperpolarization to adaptation and conduction block in sensory neurones of the leech. J. Physiol. (Lond.) 230, 509-534 (1973).
73. Yau, K. W. Receptive fields, geometry and conduction block of sensory neurons in the CNS of the leech. J. Physiol. (Lond.) 263, 513-538 (1976).
74. Gu, X. Effect of conduction block at axon bifurcations on synaptic transmission to different postsynaptic neurons in the leech. J. Physiol. (Lond.) 441, 755-778 (1991).
75. Baccus, S. A. Synaptic facilitation by reflected action potentials: enhancement of transmission when nerve impulses reverse direction at axon branch points. Proc. Natl Acad. Sci. USA 95, 8345-8350 (1998). Experimental evidence that action potential propagation might reflect at branch points of invertebrate axons. Reflected action potentials facilitates synaptic transmission.
76. Baccus, S. A., Burrell, B. D., Sahley, C. L. & Muller, K. J. Action potential reflection and failure at axon branch points cause stepwise changes in EPSPs in a neuron essential for leaming. J. Neurophysiol. 83, 1683-1700 (2000).
77. Deschênes, M. & Landry, P. Axonal branch diameter and spacing of nodes in the terminal arborization of identified thalamic and cortical neurons. Brain Res. 191, 538-544 (1980).
78. Ducreux, C., Reynaud, J. C. & Puizillout, J. J. Spike conduction properties of T-shaped C neurons in the rabbit nodose ganglion. Eur. J. Physiol. 424, 238-244 (1993).
79. Lüscher, C., Streit, J., Lipp, P. & Lüscher, H. R. Action potential propagation through embryonic dorsal root ganglion cells in culture. II. Decrease of conduction reliability during repetitive stimulation. J. Neurophysiol. 72, 634-644 (1994).
80. Dyball, R. E., Grossmann, R., Leng, G. & Shibuki, K. Spike propagation and conduction failure in rat neural lobe. J. Physiol. (Lond) 401, 241-256 (1988).
81. h might act as an homeostatic current for the conduction of repetitive action potentials.
82. Grossman, Y., Parnas, I. & Spira, M. E. Ionic mechanisms involved in differential conduction of action potentials at high frequency in a branching axon. J. Physiol. (Lond.) 295, 307-322 (1979).
83. Smith, D. O. Morphological aspects of the safety factor for action potential propagation at axon branch points. J. Physiol. (Lond.) 301, 261-269 (1980).
84. Bourque, C. W. Intraterminal recordings from the rat neurohypophysis in vitro. J. Physiol (Lond.) 421, 247-262 (1990).
85. Zhang, S. J. & Jackson, M. B. GABA-activated chloride channels in secretory nerve endings. Science 259, 531-534 (1993).
86. Jackson, M. B. & Zhang, S. J. Action potential propagation block by GABA in rat posterior pituitary nerve terminals. J. Physiol. (Lond.) 483, 597-611 (1995).
87. Antic, S., Wuskell, J. P., Loew, L. & Zecevic, D. Functional profile of the giant metacerebral neuron of Helix asperse: temporal and spatical dynamics of electrical activity in situ. J. Physiol. (Lond.) 527, 55-69 (2000). A multi-optical recording study with voltage-sensitive dyes of propagation failures in central neurons of the snail.
88. Macagno, E. R., Muller, K. J. & Pitman, R. M. Conduction block silences parts of a chemical synapse in the leech central nervous system. J. Physiol. (Lond) 387, 649-664 (1987).
89. Muller, K. J. & Scott, S. A. Transmission at a 'direct' electrical connexion mediated by an interneurone in the leech. J. Physiol. (Lond.) 311, 565-583 (1981).
90. Eng, D. L. & Kocsis, J. D. Activity-dependent changes in extracellular potassium and excitability in turtle olfactory nerve. J. Neurophysiol. 57, 185-202 (1987).
91. Poolos, N. P., Mauk, M. D. & Kocsis, J. D. Activity-evoked increases in intracellular potassium modulate presynaptic excitability in the CA1 region of the hippocampus. J. Neurophysiol. 58, 404-416 (1987).
92. Heitler, W. J. & Goodman, C. S. Multiple sites of spike initiation in a bifurcating locust neurone. J. Exp. Biol. 76, 63-84 (1978).
93. Ritchie, J. M. & Straub, R. W. The after-effects of repetitive stimulation on mammalian non-modulated fibres. J. Physiol. (Lond.) 134, 698-711 (1956).
94. Ritchie, J. M. & Straub, R. W. The hyperpolarization which follows activity in mammalian non-modulated fibres. J. Physiol. (Lond.) 138, 80-97 (1957)
95. Mar, A. & Drapeau, P. Modulation of conduction block in leech mechanosensory neurons. J. Neurosci. 16, 4335-4334 (1996).
96. +-channels and axonal geometry in the gating of action potential propagation along CA3 pyramidal cell axons: a simulation study. J. Neurosci. 18, 7436-7451 (1998).
97. Obaid, A. L. & Salzberg, B. M. Micromolar 4-aminopyridine enhances invasion of a vertebrate neurosecretary terminal arborization. J. Gen. Physiol. 107, 353-368 (1996).
98. 2+ imaging of CNS axons in culture indicate reliable coupling between single action potentials and distal functional release sites. Neuron 16, 783-795 (1996).
99. 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).
100. Raastad, M. & Shepherd, G. Single-axon action potentials in the rat hippocampal cortex. J. Physiol. (Lond.) 548, 745-752 (2003).
101. Cox, C. L., Denk, W., Tank, D. W. & Svoboda, K. Action potentials reliably invade axonal arbors of rat neocortical neurons. Proc. Natl Acad. Sci. USA 97, 9724-9728 (2000).
102. Koester, H. J. & Sakmann, B. Calcium dynamic associated with action potentials in single nerve terminals of pyramidal cells in layer 2/3 of the young rat neocortex. J. Physiol. (Lond.) 529, 625-646 (2000).
103. Debanne, D., Kopysova, I. L., Bras, H. & Ferrand, N. Gating of action potential propagation by an axonal A-like potassium conductance in the hippocampus: a new type of non-synaptic plasticity. J. Physiol. (Paris) 93, 285-296 (1999).
104. 2+ modulates information coding at CA3-CA3 synapses in the rat hippocampus. J. Physiol. (Lond.) 552, 513-524 (2003).
105. Goldstein, S. & Rail, W. Changes of action potential shape and velocity for changing core conductor geometry. Biophys. J. 14, 731-757 (1974). This theoretical paper sets the rules for the role of local axon geometry on the properties of axon conduction.
106. Ramon, F., Joyner, R. W. & Moore, J. W. Propagation of action potentials in inhomogeneous axon regions. Fed. Proc. 34, 1357-1363 (1975).
107. Parnas, I. in The Neurosciences (eds Schmitt, F. O. & Worden F. G.) 499-512 (MIT Press, Cambridge, Massachusetts, 1979).
108. Isope, P., Franconville, R., Barbour, B. & Ascher, P. Repetitive firing of rat cerebellar parallel fibres after a single stimulation. J. Physiol. (Lond.) 554, 829-839 (2004).
109. Katz, B. & Schmitt, O. Electric interaction between two adjacent nerve fibres. J. Physiol (Lond.) 97, 471-488 (1940).
110. Katz, B. & Schmitt, O. A note on interaction between nerve fibers. J. Physiol. (Lond.) 100, 369-371 (1942).
111. Arvanitaki, A. Effects evoked in an axon by the activity of a contiguous one. J. Neurophysiology 5, 89-108 (1942).
112. Kocsis, J. D., Ruiz, J. A. & Cummins, K. L. Modulation of axonal excitability mediated by surround electrical activity: an intra-axonal study. Exp. Brain Res. 47, 151-153 (1982).
113. Binczak, S., Eilbeck, J. C. & Scott, A. C. Ephaptic coupling between myelinated nerve fibers. Physicia D 148, 159-174 (2001).
114. Reutskjy, S., Rossoni, E. & Tirozzi, B. Conduction in bundles of demyelinated nerve fibers: computer simulation. Biol. Cybern. 89, 439-448 (2003).
115. Holt, G. A. & Koch, C. Electrical interactions via the extracellular potential near cell bodies. J. Comput. Neurosci. 6, 169-184 (1999).
116. Traub, R. D. et al. Axonal gap junctions between neurons: a novel source of network oscillations and perhaps epileptogenesis. Rev. Neurosci. 13, 1-30 (2002).
117. Draguhn, A., Traub, R. D., Schmitz, D. & Jefferys, J. G. R. Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394, 189-192 (1998).
118. Klausberger, T. et al. Brain-state- and cell-type-specific fidng of hippocampal interneurons in vivo. Nature 421, 844-848 (2003).
119. Schmitz, D. et al. Axo-axonal coupling: a novel mechanism for ultrafast neuronal communication. Neuron 31, 831-840 (2001). Axons of CA1 pyramidal cells are electrically coupled through gap junctions.
120. Bruzzone, R., Hormudzi, S. G., Barbe, M. T., Herb, A. & Monyer, H. Pannexins, a family of gap junction proteins expressed in brain. Proc. Natl Acad. Sci. USA 100, 13644-13649 (2003).
121. Chen, W. R., Shen, G. Y., Shepherd, G. M., Hines, M. L. & Midtgaard, J. Multiple modes of action potential initiation and propagation in mitral cell primary dendrite. J. Neurophysiol. 88, 2755-2764 (2002). First experimental evidence for reflection of action potential propagation in an axon-like dendrite of mammalian neuron.
122. Segev, I. Computer study of presynaptic inhibition controlling the spread of action potentials into axonal terminals. J. Neurophysiol. 63, 987-998 (1990).
123. Garrido, J. et al. A targeting motif that determines sodium channel clustering at the axonal initial segment. Science 300, 2091-2094 (2003).
124. v1 (Shaker) voltage-gated potassium channels. Science 301, 646-649 (2003).
125. Jay, D. G. Selective destruction of protein function by chromophore-assisted laser inactivation. Proc. Natl Acad. Sci. USA 85, 5454-5458 (1988).
126. Wong, E., David, S., Jacob, M. H. & Jay, D. G. Inactivation of myelin-associated glycoprotein enhances optic nerve regeneration. J. Neurosci. 23, 3112-3117 (2003).
127. Maex, R. & De Schutter, E. Resonant synchronization in heterogeneous networks of inhibitory neurons. J. Neurosci. 23, 10503-10514 (2003).
128. Segev, I. & Schneidman, E. Axons as computing devices: basic insights gained from models. J. Physiol. (Paris) 93, 263-270 (1999).
129. Vincent, P. & Marty, A. (1996) Fluctuations of inhibitory postsynaptic currents in Purkinje cells from rat cerebellar slices. J. Physiol. (Lond.) 494, 183-199 (1996).
130. Huguenard, J. R. Reliability of axonal propagation: the spike doesn't stop here. Proc. Natl Acad. Sci. USA. 97, 9349-9350 (2000).
131. Debanne, D. & Russier, M. Axonal propagation: does the spike stop here? J. Physiol. (Lond.) 548, 663.
132. Häusser, M., Spruston, N. & Stuart, G. J. Diversity and dynamics of dendritic signaling. Science 290, 739-744 (2000).
133. Segev, I. & London, M. Untangling dendrites with quantitative models. Science 290, 744-750 (2000)
134. Williams, S. R. & Stuart, G. J. Role of dendritic synapse location in the control of action potential output. Trends Neurosci. 26, 147-154 (2003).
135. Parnas, I., Hochstein, S. & Parnas, H. Theoretical analysis of parameters leading to frequency modulation along an inhomogeneous axon. J. Neurophysiol. 39, 909-923 (1976).
136. Lüscher, H. R. & Shiner, J. S. Computation of action potential propagation and presynaptic bouton activation in terminal arborizations of different geometries. Biophys. J. 58, 1377-1388 (1990).
137. Lüscher, H. R. & Shiner, J. S. Simulation of action potential propagation in complex terminal arborizations. Biophys. J. 58, 1389-1399 (1990).
138. Graham, B. & Redman, S. A simulation of action potentials in synaptic boutons during presynaptic inhibition. J. Neurophysiol. 71, 538-549 (1994).
139. Goldfinger, M. D. Computation of high safety factor impulse propagation at axonal branch points. NeuroReport 11, 449-456 (2000).
140. Zhou, L. & Chiu, S. Y. Computer model for action potential propagation through branch point in myelinated nerves. J. Neurophysiol. 85, 197-210 (2001).
141. Rall, W. Branching dendritic trees and motoneuron membrane resistivity. Expl. Neurol. 1, 491-527 (1959).
142. Rall, W. in Neural Theory of Modeling (ed. Reiss, F.P.) 73-97 (Standford Univ. Press, Palo Alto, 1964).
143. Chen, W. R., Midtgaard, J. & Shepherd, G. M. Forward and backward propagation of dendritic impulses and their synaptic control in mitral cells. Science 278, 463-467 (1997).
144. Bischofberger, J. & Jonas, P. Action potential propagation into the presynaptic dendrites of rat mitral cells. J. Physiol. (Lond.) 504, 350-365 (1997).
145. Velte, T. J. & Masland, R. H. Action potentials in the dendrites of retinal ganglion cells. J. Neurophysiol. 81, 1412-1417 (1999).