Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Compartmentalized dendritic plasticity and input feature storage in neurons

Abstract

Although information storage in the central nervous system is thought to be primarily mediated by various forms of synaptic plasticity, other mechanisms, such as modifications in membrane excitability, are available. Local dendritic spikes are nonlinear voltage events that are initiated within dendritic branches by spatially clustered and temporally synchronous synaptic input. That local spikes selectively respond only to appropriately correlated input allows them to function as input feature detectors and potentially as powerful information storage mechanisms. However, it is currently unknown whether any effective form of local dendritic spike plasticity exists. Here we show that the coupling between local dendritic spikes and the soma of rat hippocampal CA1 pyramidal neurons can be modified in a branch-specific manner through an N-methyl-d-aspartate receptor (NMDAR)-dependent regulation of dendritic Kv4.2 potassium channels. These data suggest that compartmentalized changes in branch excitability could store multiple complex features of synaptic input, such as their spatio-temporal correlation. We propose that this ‘branch strength potentiation’ represents a previously unknown form of information storage that is distinct from that produced by changes in synaptic efficacy both at the mechanistic level and in the type of information stored.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Two populations of dendritic spike strengths.
Figure 2: Relationship of dendritic morphology and branch strength.
Figure 3: Branch strength potentiation.
Figure 4: Specificity and associativity of branch strength potentiation.
Figure 5: BSP is mediated by reduced A-type K + channel function.

Similar content being viewed by others

References

  1. Ariav, G., Polsky, A. & Schiller, J. Submillisecond precision of the input-output transformation function mediated by fast sodium dendritic spikes in basal dendrites of CA1 pyramidal neurons. J. Neurosci. 23, 7750–7758 (2003)

    Article  CAS  Google Scholar 

  2. Larkum, M. E., Zhu, J. J. & Sakmann, B. Dendritic mechanisms underlying the coupling of the dendritic with the axonal action potential initiation zone of adult rat layer 5 pyramidal neurons. J. Physiol. (Lond.) 533, 447–466 (2001)

    Article  CAS  Google Scholar 

  3. Polsky, A., Mel, B. W. & Schiller, J. Computational subunits in thin dendrites of pyramidal cells. Nature Neurosci. 7, 621–627 (2004)

    Article  CAS  Google Scholar 

  4. Losonczy, A. & Magee, J. C. Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 50, 291–307 (2006)

    Article  CAS  Google Scholar 

  5. Gasparini, S., Migliore, M. & Magee, J. C. On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. J. Neurosci. 24, 11046–11056 (2004)

    Article  CAS  Google Scholar 

  6. Gasparini, S. & Magge, J. C. State-dependent dendritic computation in hippocampal CA1 pyramidal neurons. J. Neurosci. 26, 2088–2100 (2006)

    Article  CAS  Google Scholar 

  7. Poirazi, P., Brannon, T. & Mel, B. W. Pyramidal neuron as two-layer neural network. Neuron 37, 989–999 (2003)

    Article  CAS  Google Scholar 

  8. Poirazi, P. & Mel, B. W. Impact of active dendrites and structural plasticity on the memory capacity of neural tissue. Neuron 29, 779–796 (2001)

    Article  CAS  Google Scholar 

  9. London, M. & Hausser, M. Dendritic computation. Annu. Rev. Neurosci. 28, 503–532 (2005)

    Article  CAS  Google Scholar 

  10. Zhang, W. & Linden, D. J. The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nature Rev. Neurosci. 4, 885–900 (2003)

    Article  ADS  CAS  Google Scholar 

  11. Magee, J. C. & Johnston, D. Plasticity of dendritic function. Curr. Opin. Neurobiol. 15, 334–342 (2006)

    Article  Google Scholar 

  12. Frick, A., Magee, J. C. & Johnston, D. LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nature Neurosci. 7, 126–135 (2004)

    Article  CAS  Google Scholar 

  13. Yasuda, R. et al. Supersensitive Ras activation in dendrites and spines revealed by two-photon fluorescent lifetime imaging. Nature Neurosci. 9, 283–291 (2006)

    Article  CAS  Google Scholar 

  14. Kim, J., Jung, S. C., Clemens, C. M., Petralia, R. S. & Hoffman, D. A. Regulation of dendritic excitability by activity-dependent trafficking of the A-type K+ channel subunit Kv4.2 in hippocampal neurons. Neuron 54, 933–947 (2007)

    Article  CAS  Google Scholar 

  15. Golding, N. L. & Spruston, N. Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 21, 1189–1200 (1998)

    Article  CAS  Google Scholar 

  16. Bannister, N. J. & Larkmann, A. U. Dendritic morphology of CA1 pyramidal neurones from the rat hippocampus: I. Branching patterns. J. Comp. Neurol. 360, 150–160 (1995)

    Article  CAS  Google Scholar 

  17. Ishizuka, N., Weber, J. & Amaral, D. Organization of intrahippocampal projections orginating from CA3 pyramidal cells of the rat. J. Comp. Neurol. 295, 580–623 (1990)

    Article  CAS  Google Scholar 

  18. Csicsvari, J., Hirase, H., Czurko, A., Mamiya, A. & Buzsaki, G. Ensemble patterns of hippocampal CA3–CA1 neurons during sharp wave-associated population events. Neuron 28, 585–594 (2000)

    Article  CAS  Google Scholar 

  19. O’Neill, J., Senior, T. & Csicsvari, J. Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron 49, 143–156 (2006)

    Article  Google Scholar 

  20. Hasselmo, M. E. & Giocomo, L. M. Cholinergic modulation of cortical function. J. Mol. Neurosci. 30, 133–135 (2006)

    Article  CAS  Google Scholar 

  21. Gasparini, S., Losonczy, A., Chen, X., Johnston, D. & Magee, J. C. Associative pairing enhances action potential back-propagation in radial oblique branches of CA1 pyramidal neurons. J. Physiol. (Lond.) 580, 787–800 (2007)

    Article  CAS  Google Scholar 

  22. Hoffman, D. A. & Johnston, D. Neuromodulation of dendritic action potentials. J. Neurophysiol. 81, 408–411 (1999)

    Article  CAS  Google Scholar 

  23. Chen, X. et al. Deletion of Kv4.2 gene eliminates dendritic A-type K+ current and enhances induction of long-term potentiation in hippocampal CA1 pyramidal neurons. J. Neurosci. 26, 12143–12151 (2006)

    Article  CAS  Google Scholar 

  24. Guo, W. et al. Targeted deletion of Kv4.2 eliminates Ito,f and results in electrical and molecular remodeling, with no evidence of ventricular hypertrophy or myocardial dysfunction. Circ. Res. 97, 1342–1350 (2005)

    Article  CAS  Google Scholar 

  25. Govindarajan, A., Kelleher, R. J. & Tonegawa, S. Clustered plasticity model of long-term memory engrams. Nature Rev. Neurosci. 7, 575–583 (2006)

    Article  CAS  Google Scholar 

  26. Harvey, C. D. & Svoboda, K. Spatially clustered and dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 450, 1195–1200 (2007)

    Article  ADS  CAS  Google Scholar 

  27. Fusi, S., Drew, P. J. & Abbott, L. F. Cascade models of synaptically stored memories. Neuron 45, 599–611 (2005)

    Article  CAS  Google Scholar 

  28. Wilson, M. A. & McNaughton, B. L. Reactivation of hippocampal ensemble memories during sleep. Science 265, 676–679 (1994)

    Article  ADS  CAS  Google Scholar 

  29. Nadasdy, Z., Hirase, H., Czurko, A., Csicsvari, J. & Buzsaki, G. Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 19, 9497–9507 (1999)

    Article  CAS  Google Scholar 

  30. Lee, A. K. & Wilson, M. A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 1183–1194 (2002)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank G. Buzsaki, D. Johnston, J. Lisman and Z. Nusser for their comments on a previous version of the manuscript. We thank D. Johnston for the Kv.4.2 mice and B. K. Andrasfalvy for valuable discussions and help with experiments using Kv4.2 mice.

Author Contributions A.L. and J.K.M. performed and analysed the experiments, A.L., J.K.M. and J.C.M. designed the experiments, and all authors contributed to the manuscript preparation.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Attila Losonczy or Judit K. Makara.

Supplementary information

Supplementary Figures

The file contains Supplementary Figures 1-6 with Legends. (PDF 5759 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Losonczy, A., Makara, J. & Magee, J. Compartmentalized dendritic plasticity and input feature storage in neurons. Nature 452, 436–441 (2008). https://doi.org/10.1038/nature06725

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature06725

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing