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PMID: 15590929 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Boosting of action potential backpropagation by neocortical network activity in vivo.

Waters J, Helmchen F

Abstract

Action potentials backpropagate into the dendritic trees of pyramidal neurons, reporting output activity to the sites of synaptic input and provoking long-lasting changes in synaptic strength. It is unclear how this retrograde signal is modified by neural network activity. Using whole-cell recordings from somata, apical trunks, and dendritic tuft branches of layer 2/3 pyramidal neurons in vivo, we show that network-driven subthreshold membrane depolarizations ("up states") occur simultaneously throughout the apical dendritic tree. This spontaneous synaptic activity enhances action potential-evoked calcium influx into the distal apical dendrite by promoting action potential backpropagation. Hence, somatic feedback to the dendrites becomes stronger with increasing network activity.

MeSH Terms
Action Potentials/physiology Animals Calcium/metabolism,physiology Dendrites/physiology Electroencephalography Neocortex/physiology Nerve Net/physiology Pyramidal Cells/physiology Rats Rats, Wistar Signal Processing, Computer-Assisted Synapses/physiology
Chemicals
Calcium
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Waters Jack
Abteilung Zellphysiologie, Max-Planck-Institut für medizinische Forschung, 69120 Heidelberg, Germany. jwaters@mpimf-heidelberg.mpg.de
Helmchen Fritjof
References (43)
43 references, click to expand
  1. Synchronous membrane potential fluctuations in neurons of the cat visual cortex.
    Neuron. 1999 Feb;22(2):361-74 PMID: 10069341
  2. A new cellular mechanism for coupling inputs arriving at different cortical layers.
    Nature. 1999 Mar 25;398(6725):338-41 PMID: 10192334
  3. Spread of dendritic excitation in layer 2/3 pyramidal neurons in rat barrel cortex in vivo.
    Nat Neurosci. 1999 Jan;2(1):65-73 PMID: 10195182
  4. NMDA receptor-mediated subthreshold Ca(2+) signals in spines of hippocampal neurons.
    J Neurosci. 2000 Mar 1;20(5):1791-9 PMID: 10684880
  5. Columnar organization of dendrites and axons of single and synaptically coupled excitatory spiny neurons in layer 4 of the rat barrel cortex.
    J Neurosci. 2000 Jul 15;20(14):5300-11 PMID: 10884314
  6. Diversity and dynamics of dendritic signaling.
    Science. 2000 Oct 27;290(5492):739-44 PMID: 11052929
  7. Dendritic coincidence detection of EPSPs and action potentials.
    Nat Neurosci. 2001 Jan;4(1):63-71 PMID: 11135646
  8. Odor-evoked calcium signals in dendrites of rat mitral cells.
    Proc Natl Acad Sci U S A. 2001 Jan 30;98(3):1230-4 PMID: 11158622
  9. Subthreshold inactivation of Na+ and K+ channels supports activity-dependent enhancement of back-propagating action potentials in hippocampal CA1.
    J Neurophysiol. 2001 Feb;85(2):1013-6 PMID: 11160533
  10. Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study.
    Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):1924-9 PMID: 11172052
  11. Natural waking and sleep states: a view from inside neocortical neurons.
    J Neurophysiol. 2001 May;85(5):1969-85 PMID: 11353014
  12. Impact of network activities on neuronal properties in corticothalamic systems.
    J Neurophysiol. 2001 Jul;86(1):1-39 PMID: 11431485
  13. Influence of dendritic conductances on the input-output properties of neurons.
    Annu Rev Neurosci. 2001;24:653-75 PMID: 11520915
  14. The life cycle of Ca(2+) ions in dendritic spines.
    Neuron. 2002 Jan 31;33(3):439-52 PMID: 11832230
  15. Dendritic calcium encodes striatal neuron output during up-states.
    J Neurosci. 2002 Mar 1;22(5):1499-512 PMID: 11880480
  16. Dynamic gating of spike propagation in the mitral cell lateral dendrites.
    Neuron. 2002 Mar 28;34(1):115-26 PMID: 11931746
  17. Emerging rules for the distributions of active dendritic conductances.
    Nat Rev Neurosci. 2002 May;3(5):362-70 PMID: 11988775
  18. Spike timing, calcium signals and synaptic plasticity.
    Curr Opin Neurobiol. 2002 Jun;12(3):305-14 PMID: 12049938
  19. In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain.
    Pflugers Arch. 2002 Jul;444(4):491-8 PMID: 12136268
  20. Ca2+ imaging in the mammalian brain in vivo.
    Eur J Pharmacol. 2002 Jul 5;447(2-3):119-29 PMID: 12151004
  21. Molecular physiology of low-voltage-activated t-type calcium channels.
    Physiol Rev. 2003 Jan;83(1):117-61 PMID: 12506128
  22. A fast-conducting, stochastic integrative mode for neocortical neurons in vivo.
    J Neurosci. 2003 Mar 15;23(6):2466-76 PMID: 12657707
  23. Dynamic receptive fields of reconstructed pyramidal cells in layers 3 and 2 of rat somatosensory barrel cortex.
    J Physiol. 2003 Nov 15;553(Pt 1):243-65 PMID: 12949232
  24. Distance-dependent modifiable threshold for action potential back-propagation in hippocampal dendrites.
    J Neurophysiol. 2003 Sep;90(3):1807-16 PMID: 12966178
  25. Supralinear Ca2+ influx into dendritic tufts of layer 2/3 neocortical pyramidal neurons in vitro and in vivo.
    J Neurosci. 2003 Sep 17;23(24):8558-67 PMID: 13679425
  26. Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex.
    Proc Natl Acad Sci U S A. 2003 Nov 11;100(23):13638-43 PMID: 14595013
  27. Action potential timing determines dendritic calcium during striatal up-states.
    J Neurosci. 2004 Jan 28;24(4):877-85 PMID: 14749432
  28. Backpropagating action potentials in neurones: measurement, mechanisms and potential functions.
    Prog Biophys Mol Biol. 2005 Jan;87(1):145-70 PMID: 15471594
  29. Characterization of single voltage-gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons.
    J Physiol. 1995 Aug 15;487(1):67-90 PMID: 7473260
  30. Different Ca2+ channels in soma and dendrites of hippocampal pyramidal neurons mediate spike-induced Ca2+ influx.
    J Neurophysiol. 1995 Jun;73(6):2553-7 PMID: 7666160
  31. Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex.
    J Neurosci. 1994 Feb;14(2):751-62 PMID: 7905516
  32. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites.
    Nature. 1994 Jan 6;367(6458):69-72 PMID: 8107777
  33. Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex.
    J Neurophysiol. 1994 Jan;71(1):17-32 PMID: 8158226
  34. A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components.
    J Neurosci. 1993 Aug;13(8):3252-65 PMID: 8340806
  35. Facilitation of Ca2+ current in excitable cells.
    Trends Neurosci. 1996 Jan;19(1):35-43 PMID: 8787140
  36. IPSPs modulate spike backpropagation and associated [Ca2+]i changes in the dendrites of hippocampal CA1 pyramidal neurons.
    J Neurophysiol. 1996 Nov;76(5):2896-906 PMID: 8930242
  37. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons.
    Science. 1997 Jan 10;275(5297):209-13 PMID: 8985013
  38. In vivo dendritic calcium dynamics in neocortical pyramidal neurons.
    Nature. 1997 Jan 9;385(6612):161-5 PMID: 8990119
  39. Action potential initiation and backpropagation in neurons of the mammalian CNS.
    Trends Neurosci. 1997 Mar;20(3):125-31 PMID: 9061867
  40. Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo.
    J Neurophysiol. 1997 Apr;77(4):1697-715 PMID: 9114230
  41. Backward cortical projections to primary somatosensory cortex in rats extend long horizontal axons in layer I.
    J Comp Neurol. 1998 Jan 12;390(2):297-310 PMID: 9453672
  42. Action potential initiation and propagation in rat neocortical pyramidal neurons.
    J Physiol. 1997 Dec 15;505 ( Pt 3):617-32 PMID: 9457640
  43. Somadendritic backpropagation of action potentials in cortical pyramidal cells of the awake rat.
    J Neurophysiol. 1998 Mar;79(3):1587-91 PMID: 9497436
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2004-12-08
Pages
11127-36
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6730284
Subset
IM
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