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Properties of basal dendrites of layer 5 pyramidal neurons: a direct patch-clamp recording study

Nature Neuroscience volume 10, pages 206–214 (2007)Cite this article

Abstract

Basal dendrites receive the majority of synapses that contact neocortical pyramidal neurons, yet our knowledge of synaptic processing in these dendrites has been hampered by their inaccessibility for electrical recordings. A new approach to patch-clamp recordings enabled us to characterize the integrative properties of these cells. Despite the short physical length of rat basal dendrites, synaptic inputs were electrotonically remote from the soma (>30-fold excitatory postsynaptic potential (EPSP) attenuation) and back-propagating action potentials were significantly attenuated. Unitary EPSPs were location dependent, reaching large amplitudes distally (>8 mV), yet their somatic contribution was relatively location independent. Basal dendrites support sodium and NMDA spikes, but not calcium spikes, for 75% of their length. This suggests that basal dendrites, despite their proximity to the site of action potential initiation, do not form a single basal-somatic region but rather should be considered as a separate integrative compartment favoring two integration modes: subthreshold, location-independent summation versus local amplification of incoming spatiotemporally clustered information.

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Figure 1: Attenuation of BAPs from soma to basal dendrites.
Figure 2: Measurement of unitary EPSPs and their attenuation in basal dendrites.
Figure 3: Steady-state current injection.
Figure 4: Location dependence of EPSP amplitudes in basal dendrites.
Figure 5: Local sodium spikes in basal dendrites.
Figure 6: Compartmental modeling of BAPs and dendritic sodium spikes in basal dendrites of layer 5 pyramidal neurons.
Figure 7: NMDA spikes in basal dendrites are less attenuated than subthreshold EPSPs.

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References

  1. Larkman, A.U. Dendritic morphology of pyramidal neurones of the visual cortex of the rat: III. Spine distributions. J. Comp. Neurol. 306, 332–343 (1991).

    Article  CAS  Google Scholar 

  2. Bannister, A.P. Inter- and intra-laminar connections of pyramidal cells in the neocortex. Neurosci. Res. 53, 95–103 (2005).

    Article  Google Scholar 

  3. Häusser, M., Spruston, N. & Stuart, G.J. Diversity and dynamics of dendritic signaling. Science 290, 739–744 (2000).

    Article  Google Scholar 

  4. Martina, M., Vida, I. & Jonas, P. Distal initiation and active propagation of action potentials in interneuron dendrites. Science 287, 295–300 (2000).

    Article  CAS  Google Scholar 

  5. Rapp, M., Yarom, Y. & Segev, I. Modeling back propagating action potential in weakly excitable dendrites of neocortical pyramidal cells. Proc. Natl. Acad. Sci. USA 93, 11985–11990 (1996).

    Article  CAS  Google Scholar 

  6. Larkman, A.U., Major, G., Stratford, K.J. & Jack, J.J. Dendritic morphology of pyramidal neurones of the visual cortex of the rat. IV: Electrical geometry. J. Comp. Neurol. 323, 137–152 (1992).

    Article  CAS  Google Scholar 

  7. Schiller, J., Major, G., Koester, H.J. & Schiller, Y. NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 404, 285–289 (2000).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  9. Antic, S.D. Action potentials in basal and oblique dendrites of rat neocortical pyramidal neurons. J. Physiol. 550, 35–50 (2003).

    Article  CAS  Google Scholar 

  10. Milojkovic, B.A., Radojicic, M.S., Goldman-Rakic, P.S. & Antic, S.D. Burst generation in rat pyramidal neurones by regenerative potentials elicited in a restricted part of the basilar dendritic tree. J. Physiol. 558, 193–211 (2004).

    Article  CAS  Google Scholar 

  11. 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 

  12. Kampa, B.M. & Stuart, G.J. Calcium spikes in basal dendrites of layer 5 pyramidal neurons during action potential bursts. J. Neurosci. 26, 7424–7432 (2006).

    Article  CAS  Google Scholar 

  13. 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 

  14. Zador, A.M., Agmon-Snir, H. & Segev, I. The morphoelectrotonic transform: a graphical approach to dendritic function. J. Neurosci. 15, 1669–1682 (1995).

    Article  CAS  Google Scholar 

  15. 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 

  16. Helmchen, F., Imoto, K. & Sakmann, B. Ca2+ buffering and action potential-evoked Ca2+ signaling in dendrites of pyramidal neurons. Biophys. J. 70, 1069–1081 (1996).

    Article  CAS  Google Scholar 

  17. Kampa, B., Letzkus, J.J. & Stuart, G. Requirement of dendritic calcium spikes for induction of spike-timing dependent synaptic plasticity. J. Physiol. 574, 283–290 (2006).

    Article  CAS  Google Scholar 

  18. Wimmer, V.C., Nevian, T. & Kuner, T. Targeted in vivo expression of proteins in the calyx of Held. Pflugers Arch. 449, 319–333 (2004).

    CAS  PubMed  Google Scholar 

  19. Dan, Y. & Poo, M.M. Spike timing-dependent plasticity: from synapse to perception. Physiol. Rev. 86, 1033–1048 (2006).

    Article  Google Scholar 

  20. Larkum, M.E., Zhu, J.J. & Sakmann, B. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398, 338–341 (1999).

    Article  CAS  Google Scholar 

  21. Häusser, M., Major, G. & Stuart, G.J. Differential shunting of EPSPs by action potentials. Science 291, 138–141 (2001).

    Article  Google Scholar 

  22. Stuart, G., Schiller, J. & Sakmann, B. Action potential initiation and propagation in rat neocortical pyramidal neurons. J. Physiol. 505, 617–632 (1997).

    Article  CAS  Google Scholar 

  23. 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. 533, 447–466 (2001).

    Article  CAS  Google Scholar 

  24. Jack, J.J.B., Noble, D. & Tsien, R.W. Electric Current Flow in Excitable Cells (Oxford University Press, 1975).

    Google Scholar 

  25. Schiller, J., Helmchen, F. & Sakmann, B. Spatial profile of dendritic calcium transients evoked by action potentials in rat neocortical pyramidal neurones. J. Physiol. (Lond.) 487, 583–600 (1995).

    Article  CAS  Google Scholar 

  26. Stuart, G.J. & Hausser, M. Dendritic coincidence detection of EPSPs and action potentials. Nat. Neurosci. 4, 63–71 (2001).

    Article  CAS  Google Scholar 

  27. Hoffman, D.A., Magee, J.C., Colbert, C.M. & Johnston, D.K. K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387, 869–875 (1997).

    Article  CAS  Google Scholar 

  28. Rall, W. & Rinzel, J. Branch input resistance and steady attenuation for input to one branch of a dendritic neuron model. Biophys. J. 13, 648–687 (1973).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  30. Williams, S.R. & Stuart, G.J. Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons. Science 295, 1907–1910 (2002).

    Article  CAS  Google Scholar 

  31. Berger, T., Larkum, M.E. & Lüscher, H.R. High I-h channel density in the distal apical dendrite of layer V pyramidal cells increases bidirectional attenuation of EPSPs. J. Neurophysiol. 85, 855–868 (2001).

    Article  CAS  Google Scholar 

  32. 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. 526, 571–587 (2000).

    Article  CAS  Google Scholar 

  33. Lörincz, A., Notomi, T., Tamás, G., Shigemoto, R. & Nusser, Z. Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat. Neurosci. 5, 1185–1193 (2002).

    Article  Google Scholar 

  34. Jaffe, D.B. & Carnevale, N.T. Passive normalization of synaptic integration influenced by dendritic architecture. J. Neurophysiol. 82, 3268–3285 (1999).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  36. Rhodes, P.A. & Llinas, R.R. Apical tuft input efficacy in layer 5 pyramidal cells from rat visual cortex. J. Physiol. 536, 167–187 (2001).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  38. Larkum, M.E., Kaiser, K.M. & Sakmann, B. Calcium electrogenesis in distal apical dendrites of layer 5 pyramidal cells at a critical frequency of back-propagating action potentials. Proc. Natl. Acad. Sci. USA 96, 14600–14604 (1999).

    Article  CAS  Google Scholar 

  39. Perez-Garci, E., Gassmann, M., Bettler, B. & Larkum, M.E. The GABA(B1b) Isoform Mediates Long-Lasting Inhibition of Dendritic Ca2+ Spikes in Layer 5 Somatosensory Pyramidal Neurons. Neuron 50, 603–616 (2006).

    Article  CAS  Google Scholar 

  40. Larkum, M.E. & Zhu, J.J. Signaling of layer 1 and whisker-evoked Ca2+ and Na+ action potentials in distal and terminal dendrites of rat neocortical pyramidal neurons in vitro and in vivo. J. Neurosci. 22, 6991–7005 (2002).

    Article  CAS  Google Scholar 

  41. Milojkovic, B.A., Radojicic, M.S. & Antic, S.D. A strict correlation between dendritic and somatic plateau depolarizations in the rat prefrontal cortex pyramidal neurons. J. Neurosci. 25, 3940–3951 (2005).

    Article  CAS  Google Scholar 

  42. Sjöström, P.J. & Häusser, M. A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons. Neuron 51, 227–238 (2006).

    Article  Google Scholar 

  43. Rhodes, P. The properties and implications of NMDA spikes in neocortical pyramidal cells. J. Neurosci. 26, 6704–6715 (2006).

    Article  CAS  Google Scholar 

  44. 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 

  45. Rathenberg, J., Nevian, T. & Witzemann, V. High-efficiency transfection of individual neurons using modified electrophysiology techniques. J. Neurosci. Methods 126, 91–98 (2003).

    Article  Google Scholar 

  46. Nevian, T. & Sakmann, B. Spine Ca2+ signaling in spike-timing-dependent plasticity. J. Neurosci. 26, 11001–11013 (2006).

    Article  CAS  Google Scholar 

  47. Destexhe, A., Mainen, Z.F. & Sejnowski, T.J. Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. J. Comput. Neurosci. 1, 195–230 (1994).

    Article  CAS  Google Scholar 

  48. 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 

  49. Magee, J., Hoffman, D., Colbert, C. & Johnston, D. Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. Annu. Rev. Physiol. 60, 327–346 (1998).

    Article  CAS  Google Scholar 

  50. Williams, S.R. & Stuart, G.J. Mechanisms and consequences of action potential burst firing in rat neocortical pyramidal neurons. J. Physiol. 521, 467–482 (1999).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank B. Mel, G. Major and H.R. Lüscher for their helpful comments on the manuscript and I. Segev for helpful discussions. We also thank B. Sakmann at the Max Planck Institute for Medical Research in Heidelberg for his generous supply of equipment and essential support and guidance. We thank K. Fischer for Neurolucida reconstructions of the biocytin-filled neurons and M. Kaiser for excellent technical assistance. This study was supported by the US National Institutes of Health, Israeli Science Foundation and the Rappaport Foundation (J.S.) and by the Swiss National Science Foundation, Grant Nr. PP00A-102721/1 (M.E.L.).

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Author notes

  1. Thomas Nevian and Matthew E Larkum: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Physiology, University of Berne, Bühlplatz 5, Berne, 3012, Switzerland

    Thomas Nevian & Matthew E Larkum

  2. Department of Cell Physiology, Max Planck Institute for Medical Research, Jahnstrasse 29, Heidelberg, 69120, Germany

    Thomas Nevian

  3. Department of Physiology, Technion Medical School, Bat-Galim, Haifa, 31096, Israel

    Alon Polsky & Jackie Schiller

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Contributions

T.N., M.E.L. and J.S. designed and conducted the experiments and wrote the manuscript. T.N., M.E.L., A.P. and J.S. analyzed the data. A.P. and J.S. performed the computer simulations.

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Correspondence to Jackie Schiller.

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Supplementary information

Supplementary Fig. 1

The effect of dendritic depolarization on BAP propagation to basal dendrites. (PDF 350 kb)

Supplementary Fig. 2

The effect of KA and KDR channel blockers on the BAPs in basal dendrites. (PDF 169 kb)

Supplementary Fig. 3

Forward and backward attenuation in basal and apical dendrites of L5 pyramidal neurons. (PDF 122 kb)

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Nevian, T., Larkum, M., Polsky, A. et al. Properties of basal dendrites of layer 5 pyramidal neurons: a direct patch-clamp recording study. Nat Neurosci 10, 206–214 (2007). https://doi.org/10.1038/nn1826

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