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:

Boosting of neuronal firing evoked with asynchronous and synchronous inputs to the dendrite

Abstract

Dendritic conductances have previously been shown to boost excitatory postsynaptic potentials (EPSPs). To determine whether this boosting translates to an increase in the efficacy for evoking action potentials, we injected barrages of EPSPs that simulate the inputs generated by a population of presynaptic cells into either the dendrite or the soma of pyramidal neurons in vitro. Although the individual dendritic and somatic EPSPs were identical, barrages delivered to the dendrite generated much higher firing rates. Boosting occurred when the simulated cells fired asynchronously and synchronously. This Na+-mediated boosting, which was manifested during repetitive firing, may compensate functionally for electrotonic attenuation of EPSPs.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Stimulus protocol.
Figure 2: Response to somatic injection.
Figure 3: Response to asynchronous dendritic stimulation.
Figure 4: Responses to synchronous dendritic stimulation.
Figure 5: Role of dendritic Na+ conductances.

Similar content being viewed by others

References

  1. Granit, R., Kernell, D. & Lamarre, Y. Algebraical summation in synaptic activation of motoneurones firing within the 'primary range' to injected currents. J. Physiol. (Lond.) 187, 379–399 (1966).

    Article  CAS  Google Scholar 

  2. Stuart, G. & Sakmann, B. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367, 69–72 (1994).

    Article  CAS  Google Scholar 

  3. Colbert, M. & Johnston, D. Axonal action potential initiation and Na+ channel densities in the soma and axon initial segment of subicular pyramidal neurons. J. Neurosci. 16, 6676–6686 (1996).

    Article  CAS  Google Scholar 

  4. Schwindt, P. & Crill, W. Equivalence of amplified current flowing from dendrite to soma measured by alteration of repetitive firing and by voltage clamp in layer 5 pyramidal neurons. J. Neurophysiol. 76, 3731–3739 (1996).

    Article  CAS  Google Scholar 

  5. Rall, W. Theoretical significance of dendritic trees for neuronal input-output relations. in Neural Theory and Modeling (ed. Reiss, R. F.) 73–97 (Stanford Univ. Press, Palo Alto, California, 1964).

    Google Scholar 

  6. Stuart, G. & Spruston, N. Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J. Neurosci. 18, 3501–3510 (1998).

    Article  CAS  Google Scholar 

  7. Schwindt, P. & Crill, W. Amplification of synaptic current by persistent sodium conductance in apical dendrite of neocortical neurons. J. Neurophysiol. 74, 2220–2224 (1995).

    Article  CAS  PubMed Central  Google Scholar 

  8. Magee, J. C. & Johnston, D. Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268, 301–304 (1995).

    Article  CAS  Google Scholar 

  9. Lipowsky, R., Gillessen, T. & Alzheimer, C. Dendritic Na+ channels amplify EPSPs in hippocampal CA1 pyramidal cells. J. Neurophysiol. 76, 2181–2191 (1996).

    Article  CAS  PubMed Central  Google Scholar 

  10. Gillessen, T. & Alzheimer, C. Amplification of EPSPs by low Ni2+- and amilioride-sensitive Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons. J. Neurophysiol. 77, 1639–1643 (1997).

    Article  CAS  PubMed Central  Google Scholar 

  11. Schiller, J., Schiller, Y., Stuart, G. & Sakmann, B. Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J. Physiol. (Lond.) 505, 605–616 (1997).

    Article  CAS  Google Scholar 

  12. Zhu, J. J. Maturation of layer 5 neocortical pyramidal neurons: amplifying salient layer 1 and layer 4 inputs by Ca2+ action potentials in adult rat tuft dendrites. J. Physiol. (Lond.) 526, 571–587 (2000).

    Article  CAS  Google Scholar 

  13. Kang, J., Huguenard, J. R. & Prince, D. A. Development of BK channels in neocortical pyramidal neurons. J. Neurophysiol. 76, 188–198 (1996).

    Article  CAS  PubMed Central  Google Scholar 

  14. Magee, J. C. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J. Neurosci. 18, 7613–7624 (1998).

    Article  CAS  Google Scholar 

  15. Poolos, N. P. & Johnston, D. Calcium-activated potassium conductances contribute to action potential repolarization at the soma but not the dendrites of hippocampal CA1 pyramidal neurons. J. Neurosci. 19, 5205–5212 (1999).

    Article  CAS  PubMed Central  Google Scholar 

  16. Bekkers, J. M. Distribution and activation of voltage-gated potassium channels in cell-attached and outside-out patches from large layer 5 cortical pyramidal neurons of the rat. J. Physiol. (Lond.) 525, 611–620 (2000).

    Article  CAS  Google Scholar 

  17. Korngreen, A. & Sakmann, B. Voltage-gated K+ channels in layer 5 neocortical pyramidal neurones from young rats: subtypes and gradients. J. Physiol. (Lond.) 525, 621–639 (2000).

    Article  CAS  Google Scholar 

  18. Williams, S. R. & Stuart, G. J. Site independence of EPSP time course is mediated by dendritic Ih in neocortical pyramidal neurons. J. Neurophysiol. 83, 3177–3182 (2000).

    Article  CAS  Google Scholar 

  19. Reyes, A. D. Influence of dendritic conductances on the input-output properties of neurons. Annu. Rev. Neurosci. 24, 653–675 (2001).

    Article  CAS  Google Scholar 

  20. Softky, W. Sub-millisecond coincidence detection in active dendritic trees. Neuroscience 58, 13–41 (1994).

    Article  CAS  Google Scholar 

  21. Reyes, A. D., Rubel, E. W. & Spain, W. J. In vitro analysis of optimal stimuli for phase-locking and time-delayed modulation of firing in avian nucleus laminaris neurons. J. Neurosci. 16, 993–1007 (1996).

    Article  CAS  PubMed Central  Google Scholar 

  22. Ferster, D. & Spruston, N. Cracking the neuronal code. Science 270, 756–757 (1995).

    Article  CAS  PubMed Central  Google Scholar 

  23. Shadlen, M. N. & Newsome, W. T. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J. Neurosci. 18, 3870–3896 (1998).

    Article  CAS  PubMed Central  Google Scholar 

  24. Borst, A. & Theunissen, F. E. Information theory and neural coding. Nature Neurosci. 2, 947–957 (1999).

    Article  CAS  PubMed Central  Google Scholar 

  25. Stevens, C. F. & Zador, A. M. Input synchrony and the irregular firing of cortical neurons. Nature Neurosci. 1, 210–217 (1998).

    Article  CAS  PubMed Central  Google Scholar 

  26. Reyes, A. D. & Sakmann, B. Developmental switch in the short-term modification of unitary EPSPs evoked in layer 2/3 and layer 5 pyramidal neurons of rat neocortex. J. Neurosci. 19, 3827–3835 (1999).

    Article  CAS  PubMed Central  Google Scholar 

  27. Magee, J. C. & Cook, E. P. Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nature Neurosci. 3, 895–903 (2000).

    Article  CAS  PubMed Central  Google Scholar 

  28. Stuart, G. & Sakmann, B. Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron 15, 1065–1076 (1995).

    Article  CAS  PubMed Central  Google Scholar 

  29. Colbert, C. M., Magee, J. C., Hoffman, D. A. & Johnston, D. Slow recovery from inactivation of Na+ channels underlies the activity-dependent attenuation of dendritic action potentials in hippocampal CA1 pyramidal neurons. J. Neurosci. 17, 6512–6521 (1997).

    Article  CAS  Google Scholar 

  30. Mickus, T., Jung, H. Y. & Spruston, N. Properties of slow, cumulative sodium channel inactivation in rat hippocampal CA1 pyramidal neurons. Biophys. J. 76, 846–860 (1999).

    Article  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank L. Abbott, F. Chance, A. Movshon and J. Rinzel for providing helpful comments. This work was supported by NSF grant IBN-0079619 (A.D.R.) and by an NSF Minority Fellowship (H.O.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alex D. Reyes.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Oviedo, H., Reyes, A. Boosting of neuronal firing evoked with asynchronous and synchronous inputs to the dendrite. Nat Neurosci 5, 261–266 (2002). https://doi.org/10.1038/nn807

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn807

This article is cited by

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