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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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).
Bannister, A.P. Inter- and intra-laminar connections of pyramidal cells in the neocortex. Neurosci. Res. 53, 95–103 (2005).
Häusser, M., Spruston, N. & Stuart, G.J. Diversity and dynamics of dendritic signaling. Science 290, 739–744 (2000).
Martina, M., Vida, I. & Jonas, P. Distal initiation and active propagation of action potentials in interneuron dendrites. Science 287, 295–300 (2000).
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).
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).
Schiller, J., Major, G., Koester, H.J. & Schiller, Y. NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 404, 285–289 (2000).
Polsky, A., Mel, B.W. & Schiller, J. Computational subunits in thin dendrites of pyramidal cells. Nat. Neurosci. 7, 621–627 (2004).
Antic, S.D. Action potentials in basal and oblique dendrites of rat neocortical pyramidal neurons. J. Physiol. 550, 35–50 (2003).
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).
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).
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).
Poirazi, P. & Mel, B.W. Impact of active dendrites and structural plasticity on the memory capacity of neural tissue. Neuron 29, 779–796 (2001).
Zador, A.M., Agmon-Snir, H. & Segev, I. The morphoelectrotonic transform: a graphical approach to dendritic function. J. Neurosci. 15, 1669–1682 (1995).
Losonczy, A. & Magee, J.C. Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 50, 291–307 (2006).
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).
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).
Wimmer, V.C., Nevian, T. & Kuner, T. Targeted in vivo expression of proteins in the calyx of Held. Pflugers Arch. 449, 319–333 (2004).
Dan, Y. & Poo, M.M. Spike timing-dependent plasticity: from synapse to perception. Physiol. Rev. 86, 1033–1048 (2006).
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).
Häusser, M., Major, G. & Stuart, G.J. Differential shunting of EPSPs by action potentials. Science 291, 138–141 (2001).
Stuart, G., Schiller, J. & Sakmann, B. Action potential initiation and propagation in rat neocortical pyramidal neurons. J. Physiol. 505, 617–632 (1997).
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).
Jack, J.J.B., Noble, D. & Tsien, R.W. Electric Current Flow in Excitable Cells (Oxford University Press, 1975).
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).
Stuart, G.J. & Hausser, M. Dendritic coincidence detection of EPSPs and action potentials. Nat. Neurosci. 4, 63–71 (2001).
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).
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).
Magee, J.C. & Cook, E.P. Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nat. Neurosci. 3, 895–903 (2000).
Williams, S.R. & Stuart, G.J. Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons. Science 295, 1907–1910 (2002).
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).
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).
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).
Jaffe, D.B. & Carnevale, N.T. Passive normalization of synaptic integration influenced by dendritic architecture. J. Neurophysiol. 82, 3268–3285 (1999).
Gasparini, S. & Magee, J.C. State-dependent dendritic computation in hippocampal CA1 pyramidal neurons. J. Neurosci. 26, 2088–2100 (2006).
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).
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).
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).
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).
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).
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).
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).
Rhodes, P. The properties and implications of NMDA spikes in neocortical pyramidal cells. J. Neurosci. 26, 6704–6715 (2006).
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).
Rathenberg, J., Nevian, T. & Witzemann, V. High-efficiency transfection of individual neurons using modified electrophysiology techniques. J. Neurosci. Methods 126, 91–98 (2003).
Nevian, T. & Sakmann, B. Spine Ca2+ signaling in spike-timing-dependent plasticity. J. Neurosci. 26, 11001–11013 (2006).
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).
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).
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).
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).
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.).
The authors declare no competing financial interests.
The effect of dendritic depolarization on BAP propagation to basal dendrites. (PDF 350 kb)
The effect of KA and KDR channel blockers on the BAPs in basal dendrites. (PDF 169 kb)
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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