Submillisecond precision of the input-output transformation function mediated by fast sodium dendritic spikes in basal dendrites of CA1 pyramidal neurons

Journal of Neuroscience

Volumn 23, Issue 21, 2003, Pages 7750-7758

  Ariav, Gal ^a   Polsky, Alon ^a   Schiller, Jackie ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Cortex; Dendrites; Spike; Submillisecond; Synaptic integration; Temporal coding

Indexed keywords

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CHANNEL GATING; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SPIKE WAVE; SYNAPTIC TRANSMISSION;

EID: 0041319178     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-21-07750.2003     Document Type: Article

References (68)

1. Abeles M (1990) Corticonics. Cambridge, UK: Cambridge UP.
2. Archie KA, Mel BW (2000) A model for intradendritic computation of binocular disparity. Nat Neurosci 3:54-63.
3. Arieli A, Sterkin A, Grinvald A, Aertsen A (1996) Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 273:1868-1871.
4. Azouz R, Gray CM (1999) Cellular mechanisms contributing to response variability of cortical neurons in vivo. J Neurosci 19:2209-2223.
5. Azouz R, Gray CM (2000) Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. Proc Natl Acad Sci USA 97:8110-8115.
6. Bernander O, Douglas RJ, Martin KA, Koch C (1991) Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc Natl Acad Sci USA 88:11569-11573.
7. Bialek W, Rieke F (1992) Reliability and information transmission in spiking neurons. Trends Neurosci 15:428-434.
8. Cash S, Yuste R (1999) Linear summation of excitatory inputs by CA1 pyramidal neurons. Neuron 22:383-394.
9. + channels underlies the activity-dependent attenuation of dendritic action potentials in hippocampal CA1 pyramidal neurons. J Neurosci 17:6512-6521.
10. deCharms RC, Zador A (2000) Neural representation and the cortical code. Annu Rev Neurosci 23:613-647.
11. Destexhe A, Pare D (1999) Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J Neurophysiol 81:1531-1547.
12. Destexhe A, Mainen ZF, Sejnowski TJ (1994) Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. J Comput Neurosci 1:195-230.
13. Golding NL, Spruston N (1998) Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 21:1189-1200.
14. Golding NL, Staff NP, Spruston N (2002) Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418:326-331.
15. Harris KD, Henze DA, Hirase H, Leinekugel X, Dragoi G, Czurko A, Buzsaki G (2002) Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417:738-741.
16. Hausser M, Spruston N, Stuart GJ (2000) Diversity and dynamics of dendritic signaling. Science 290:739-744.
17. Helmchen F, Svoboda K, Denk W, Tank DW 1999) In-Vivo dendritic calcium dynamics in deep-layer cortical pyramidal neurons. Nat Neurosci 2:989-996.
18. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179-1209.
19. Ho N, Destexhe A (2000) Synaptic background activity enhances the responsiveness of neocortical pyramidal neurons. J Neurophysiol 84:1488-1496.
20. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387:869-875.
21. Hopfield JJ (1995) Pattern recognition computations using action potential timing for stimulus representation. Nature 376:33-36.
22. Kamondi A, Acsady L, Buzsaki G (1998) Dendritic spikes are enhanced by cooperative network activity in the intact hippocampus. J Neurosci 18:3919-3928.
23. Larkum ME, Zhu JJ, Sakmann B (1999) A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398:338-341.
24. Lecar H, Nossal R (1971a) Theory of threshold fluctuations in nerves. I. Relationships between electrical noise and fluctuations in axon firing. Biophys J 11:1048-1067.
25. Lecar H, Nossal R (1971b) Theory of threshold fluctuations in nerves. II. Analysis of various sources of membrane noise. Biophys J 11:1068-1084.
26. MacVicar BA, Dudek FE (1981) Post-natal development of electrophysiological properties of art cerebral cortical pyramidal neurons. J Physiol (Lond) 393:743-762.
27. Magee JC (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18:7613-7624.
28. Magee JC (2000) Dendritic integration of excitatory synaptic input. Nat Rev Neurosci 1:181-190.
29. Magee J, Hoffman D, Colbert C, Johnston D (1998) Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. Annu Rev Physiol 60:327-346.
30. Mainen ZF, Sejnowski TJ (1995) Reliability of spike timing in neocortical neurons. Science 268:1503-1506.
31. Marsalek P, Koch C, Maunsell J (1997) On the relationship between synaptic input and spike output jitter in individual neurons. Proc Natl Acad Sci USA 21:735-740.
32. Mechler F, Victor JD, Purpura KP, Shapley R (1998) Robust temporal coding of contrast by VI neurons for transient but not for steady-state stimuli. J Neurosci 18:6583-6598.
33. Mehta MR, Lee AK, Wilson MA (2002) Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417:741-746.
34. Mel BW (1993) Synaptic integration in an excitable dendritic tree. J Neurophysiol 70:1086-1101.
35. Mel BW (1999) Why have dendrites? A computational perspective. In: Dendrites (Stuart G, Spruston N, Hausser M, eds), pp 271-289. New York: Oxford UP.
36. Poirazi P, Mel BW (2001) Impact of active dendrites and structural plasticity on the memory capacity of neural tissue. Neuron 29:779-796.
37. Migliore M, Shepherd GM (2002) Emerging rules for the distributions of active dendritic conductances. Nat Rev Neurosci 3:362-370.
38. Oviedo H, Reyes AD (2002) Boosting of neuronal firing evoked with asynchronous and synchronous inputs to the dendrite. Nat Neurosci 5:261-266.
39. Pare D, Shink E, Gaudreau H, Destexhe A, Lang EJ (1998) Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons in vivo. J Neurophysiol 79:1450-1460.
40. Rall W, Segev I (1987) Functional possibilities for synapses on dendrites and on dendritic spines. In: Synaptic function (Edelman G, Gall W, Cowan W, eds), pp 605-636. New York: Wiley.
41. Reyes A (2001) Influence of dendritic conductances on the input-output properties of neurons. Annu Rev Neurosci 24:653-675.
42. Richmond BJ, Optican LM (1987) Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. II. Quantification of response waveform. J Neurophysiol 57:147-161.
43. Richmond BJ. Optican LM. Podell M, Spitzer H (1987) Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. I. Response characteristics. J Neurophysiol 57:132-146.
44. Riehle A, Grun S, Diesmann M, Aertsen A (1997) Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278:1950-1953.
45. Rieke F, Warland D, Bialek W (1997) Spikes: exploring the neural code. Cambridge, MA: MIT.
46. Roelfsema PR, Engel AK, Konig P, Singer W (1997) Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385:157-161.
47. Schiller J, Schiller Y (2001) NMDA receptor-mediated dendritic spikes and coincident signal amplification. Curr Opin Neurobiol 11:343-348.
48. Schiller J, Schiller Y, Stuart G, Sakmann B (1997) Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J Physiol (Lond) 505:605-616.
49. Schiller J, Schiller Y, Clapham DE (1998) NMDA receptors amplify calcium influx into dendritic spines during associative pre- and postsynaptic activation. Nat Neurosci 1:114-118.
50. Schiller J, Major G, Koester HJ, Schiller Y (2000) NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 404:285-289.
51. Schmitz D, Schuchmann S, Fisahn A, Draguhn A, Buhl EH, Petrasch-Parwez E, Dermietzel R, Heinemann U, Traub RD (2001) Axo-axonal coupling. A novel mechanism for ultrafast neuronal communication. Neuron 31:831-840.
52. Schwindt PC, Crill WE (1995) Amplification of synaptic current by persistent sodium conductance in apical dendrite of neocortical neurons. J Neurophysiol 74:2220-2224.
53. Shadlen MN, Newsome WT (1994) Noise, neural codes and cortical organization. Curr Opin Neurobiol 4:569-579.
54. Shadlen MN, Newsome WT (1998) The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci 18:3870-3896.
55. Shepherd GM, Brayton R (1987) Logic operations are properties of computer-simulated interactions between excitable dendritic spines. Neuroscience 21:151-165.
56. Singer W (1999) Neuronal synchrony: a versatile code for the definition of relations? Neuron 24:49-65.
57. Softky W (1994) Sub-millisecond coincidence detection in active dendritic trees. Neuroscience 58:13-41.
58. Softky WR, Koch C (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13:334-350.
59. Spencer WA, Kandel ER (1968) Cellular and integrative properties of the hippocampal pyramidal cell and the comparative electrophysiology of cortical neurons. Int J Neurol 6:266-296.
60. Steinmetz PN, Manwani A, Koch C, London M, Segev I (2000) Subthreshold voltage noise due to channel fluctuations in active neuronal membranes. J Comput Neurosci 9:133-148.
61. Stevens CF, Zador AM (1998) Input synchrony and the irregular firing of cortical neurons. Nat Neurosci 1:210-217.
62. Stuart G, Schiller J, Sakmann B (1997) Action potential initiation and propagation in rat neocortical pyramidal neurons. J Physiol (Lond) 505:617-632.
63. Trussell LO (1999) Synaptic mechanisms for coding timing in auditory neurons. Annu Rev Physiol 61:477-496.
64. Vaadia E, Haalman I, Abeles M, Bergman H, Prut Y, Slovin H, Aertsen A (1995) Dynamics of neuronal interactions in monkey cortex in relation to behavioral events. Nature 373:515-518.
65. Valiante TA, Velazquez JLP, Jahromi SS, Carlen PL (1995) Coupling potentials in CA1 neurons during calcium-free induced field burst activity. J Neurosci 15:6946-6956.
66. Van Vreeswijk C, Sompolinsky H (1998) Chaos in neuronal networks with balanced excitatory and inhibitory activity. Science 274:1724-1726.
67. Wei D-S, Mei Y-A, Bagal A, Kao JPY, Thompson SM, Tang C-M (2001) Compartmentalized and binary behavior of terminal dendrites in hippocampal pyramidal neurons. Science 293:2272-2275.
68. Williams SR, Stuart GJ (2002) Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons. Science 295:1907-1910.