Abstract
Dendrites of CA1 pyramidal cells of the hippocampus, along with those of a wide range of other cell types, support active backpropagation of axonal action potentials. Consistent with previous work, recent experiments demonstrating that properties of synaptic plasticity are different for distal synapses, suggest an important functional role of bAPs, which are known to be prone to failure in distal locations. Using conductance-based models of CA1 pyramidal cells, we show that underlying “traveling wave attractors” control action potential propagation in the apical dendrites. By computing these attractors, we dissect and quantify the effects of IA channels and dendritic morphology on bAP amplitudes. We find that non-uniform activation properties of IA can lead to backpropagation failure similar to that observed experimentally in these cells. Amplitude of forward propagation of dendritic spikes also depends strongly on the activation dynamics of IA. IA channel properties also influence transients at dendritic branch points and whether or not propagation failure results. The branching pattern in the distal apical dendrites, combined with IA channel properties in this region, ensure propagation failure in the apical tuft for a large range of IA conductance densities. At the same time, these same properties ensure failure of forward propagating dendritic spikes initiated in the distal tuft in the absence of some form of cooperativity of synaptic activation.
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Acker, C. D., Kopell, N., & White, J. A. (2003). Synchronization of strongly coupled excitatory neurons: Relating network behavior to biophysics. Journal of Computational Neuroscience, 15, 71–90.
Bi, G. Q., & Poo, M. M. (1998). Synaptic modifications in cultured hippocampal neurons: Dependence on spike timing, synaptic strength, and postsynaptic cell type. Journal of Neuroscience, 18, 10464–10472.
Dayan P., Abbott LF (2001) Theoretical neuroscience: Computational and mathematical modeling of neural systems, (p. 220). Cambridge: MIT Press.
Ermentrout, B. (2002). Simulating, analyzing, and animating dynamical systems. Philadelphia, PA: SIAM.
Frick, A., Magee, J., & Johnston, D. (2004). LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nature Neuroscience, 7, 126–135.
Froemke, R. C., Poo, M. M., & Dan, Y. (2005). Spike-timing-dependent synaptic plasticity depends on dendritic location. Nature, 434, 221–225.
Gasparini, S., & Magee, J. C. (2002). Phosphorylation-dependent differences in the activation properties of distal and proximal dendritic Na+ channels in rat CA1 hippocampal neurons. Journal of Physiology, 541, 665–672.
Gasparini, S., Migliore, M., & Magee, J. C. (2004). On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. Journal of Neuroscience, 24, 11046–11056.
Golding, N. L., Kath, W. L., & Spruston, N. (2001). Dichotomy of action-potential backpropagation in CA1 pyramidal neuron dendrites. Journal of Neurophysiology, 86, 2998–3010.
Golding, N. L., Staff, N. P., & Spruston, N. (2002). Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature, 418, 326–331.
Goldstein, S. S., & Rall, W. (1974). Changes of action potential shape and velocity for changing core conductor geometry. Biophysical Journal, 14, 731–757.
Gulledge, A. T., Kampa, B. M., & Stuart, G. J. (2005). Synaptic integration in dendritic trees. Journal of Neurobiology, 64, 75–90.
Häusser, M., Spruston, N., & Stuart, G. J. (2000). Diversity and dynamics of dendritic signaling. Science, 290, 739–744.
Hodgkin, A. L., & Huxley, A. F. (1952). A quantitative description of membrane current and its application to conduction and excitation in nerve. Journal of Physiology, 117, 500–544.
Hoffman, D. A., & Johnston, D. (1998). Downregulation of transient K+ channels in dendrites of hippocampal CA1 pyramidal neurons by activation of PKA and PKC. Journal of Neuroscience, 18, 3521–3528.
Hoffman, D. A., Magee, J. C., Colbert, C. M., & Johnston, D. (1997). K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature, 387, 869–875.
Jarsky, T., Roxin, A., Kath, W. L., & Spruston, N. (2005). Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nature Neuroscience, 8, 1667–1676.
Johnston, D., Christie, B. R., Frick, A., Gray, R., Hoffman, D. A., Schexnayder, L. K., et al. (2003). Active dendrites, potassium channels and synaptic plasticity. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 358, 667–674.
Johnston, D., Hoffman, D. A., Colbert, C. M., & Magee, J. C. (1999). Regulation of back-propagating action potentials in hippocampal neurons. Current Opinion in Neurobiology, 9, 288–292.
Magee, J. C., & Johnston, D. (1997). A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science, 275, 209–213.
Mainen, Z. F., & Sejnowski, T. J. (1996). Influence of dendritic structure on firing pattern in model neocortical neurons. Nature, 382, 363–366.
Manor, Y., Koch, C., & Segev, I. (1991). Effect of geometrical irregularities on propagation delay in axonal trees. Biophysical Journal, 60, 1424–1437.
Markram, H., Lubke, J., Frotscher, M., & Sakmann, B. (1997). Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science, 275, 213–215.
Migliore, M., Hoffman, D. A., Magee, J. C., & Johnston, D. (1999). Role of an A-type K+ conductance in the back-propagation of action potentials in the dendrites of hippocampal pyramidal neurons. Journal of Computational Neuroscience, 7, 5–15.
Rall, W. (1959). Branching dendritic trees and motoneuron membrane resistivity. Experimental Neurology, 1, 491–527.
Rhodes, K. J., Carroll, K. I., Sung, M. A., Doliveira, L. C., Monaghan, M. M., Burke, S. L., et al. (2004). KChIPs and Kv4 alpha subunits as integral components of A-type potassium channels in mammalian brain. Journal of Neuroscience, 24, 7903–7915.
Sjöstrom, P. J., & Häusser, M. (2006). A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons. Neuron, 51, 227–238.
Spruston, N., Schiller, Y., Stuart, G., & Sakmann, B. (1995). Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science, 268, 297–300.
Stuart, G. J., & Häusser, M. (2001). Dendritic coincidence detection of EPSPs and action potentials. Nature Neuroscience, 4, 63–71.
Stuart, G. J., & Sakmann, B. (1994). Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature, 367, 69–72.
Vetter, P., Roth, A., & Häusser, M. (2001). Propagation of action potentials in dendrites depends on dendritic morphology. Journal of Neurophysiology, 85, 926–937.
Weiss, T. F. (1996). Cellular biophysics. Cambridge, MA: MIT Press.
Acknowledgements
The authors would like to thank: Georgi Medvedev (Drexel University) and Eugene Wayne (Boston University) for early, stimulating input; Bard Ermentrout (University of Pittsburgh) for technical help with XPPAUT; and Jonathan Bettencourt, Kyle Lillis, and Theoden Netoff (NDL, Boston University) for feedback and help editing the final manuscript.
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Acker, C.D., White, J.A. Roles of IA and morphology in action potential propagation in CA1 pyramidal cell dendrites. J Comput Neurosci 23, 201–216 (2007). https://doi.org/10.1007/s10827-007-0028-8
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DOI: https://doi.org/10.1007/s10827-007-0028-8