Journal of Computational Neuroscience

, Volume 7, Issue 1, pp 41–53 | Cite as

Role of Calcium Electrogenesis in Apical Dendrites: Generation of Intrinsic Oscillations by an Axial Current

  • Abdelkrim Elaagouby
  • Rafael Yuste

Abstract

Dendrites are covered with conductances whose function is still mysterious. Using intracellular recording and calcium imaging, we describe an electrogenic band of calcium channels in distal apical dendrites of layer 5 pyramidal neurons (Yuste et al., 1994). We now explore the functional consequences of this distal electrogenic area with multicompartmental numerical simulations. A calcium imaging and electrophysiological database from a single neuron, recorded under blocked sodium and potassium conductances, is replicated by simulations having increased dendritic calcium current. In these models a significant axial current flows from the apical dendrite into the somatic region, activating low-threshold calcium channels and generating oscillations similar to those seen in the electrophysiological data. We propose that the distal electrogenic area in apical dendrites serves to inject current into the soma and produce intrinsic oscillatory dynamics.

fura-2 NEURON imaging plateaus neocortex 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allbritton NL, Meyer T, Stryer L (1992) Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 258: 1812–1815.Google Scholar
  2. Amitai Y, Friedman A, Connors BW, Gutnick MJ (1993) Regenerative activity in apical dendrites of pyramidal cells in neocortex. Cerebral Cortex 3: 26–38.Google Scholar
  3. Brown A, Schwindt PC, Crill WE (1993) Voltage dependence and activation kinetics of pharmacologically defined components of the high-threshold calcium current in rat neocortical neurons. J. Neurophysiol. 70: 1530–1543.Google Scholar
  4. Chagnac-Amitai Y, Luhmann H, Prince DA (1990) Burst generating and regular spiking layer 5 pyramidal neurons of rat neocortex have different morphological features. J. Comp. Neurol. 296: 598–613.Google Scholar
  5. Connors BW, Gutnick MJ (1990) Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci. 13: 99–104.Google Scholar
  6. Gray CM, Konig P, Engel AK, Singer W (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338: 334–337.Google Scholar
  7. Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260: 3440–3450.Google Scholar
  8. Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117: 500–544.Google Scholar
  9. Jaffe DB, Ross WN, Lisman JE, Lasser-Ross N, Miyakawa H, Johnston D (1994) A model for dendritic Ca2+ accumulations in hippcammpal pyramidal neurons based on fluorescence imaging measurements. J. Neurophysiol. 71: 1065–1077.Google Scholar
  10. Johnston D, Wu SM-S (1995) Foundations of Cellular Neurophysiology. MIT Press, Cambridge, MA.Google Scholar
  11. Kao JPY, Tsien RY (1988) Ca2+ binding kinetics of fura-2 and azo-1 from temperature-jum relaxation measurements. Biophys. J. 53: 635–639.Google Scholar
  12. Kim HG, Connors BW (1993) Apical dendrites of the neocortex: Correlation between sodium-and calcium-dependent spiking and pyramidal cell morphology. J. Neurosci. 13: 5301–5311.Google Scholar
  13. Latorre R, Oberhauser A, Labarca P, Alvarez O (1989) Varieties of calcium-activated potassium channels. Ann. Rev. Physiol. 51: 385–399.Google Scholar
  14. Llinás R, Yarom Y (1981) Properties and distribution of ionic conductances generating electroresponsiveness of mammalian inferior olivary neurones in vitro. J. Physiol. (Lond.) 315: 569–584.Google Scholar
  15. Magee JC, Johnston D (1995) Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268: 301–304.Google Scholar
  16. Markram H, Sakmann B (1994) Calcium transients in apical dendrites evoked by single sub-threshold excitatory post-synaptic potentials via low voltage-activated calcium channels. Proc. Natl. Acad. Sci. USA 91: 5207–5211.Google Scholar
  17. Mason A, Larkman A (1990) Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology. J. Neurosci. 10: 1415–1428.Google Scholar
  18. Pinsky PF, Rinzel J (1994) Intrinsic and network rhythmogenesis in a reduced Traub model for CA3 neurons. J. Comput. Neurosci. 1: 39–60.Google Scholar
  19. Pockberger H (1991) Electrophysiological and morphological properties of rat motor cortex neurons in vivo. Brain Res. 539: 181–190.Google Scholar
  20. Ramón y Cajal S (1904) La Textura del Sistema Nerviosa del Hombre y los Vertebrados. Moya, Madrid.Google Scholar
  21. Regehr WG, Tank DW (1992) Calcium concentration dynamics produced by synaptic activation of CA1 hippocampal pyramidal cells. J. Neurosci. 12: 4202–4223.Google Scholar
  22. Reuveni I, Friedman A, Amitai Y, Gutnick MJ (1993) Stepwise repolarization from Ca2+ plateaus in neocortical pyramidal cells: Evidence for nonhomogeneous distribution of HVA Ca2+ channels in dendrites. J. Neurosci. 13: 4609–4621.Google Scholar
  23. Rhodes PA, Gray CM (1994) Simulations of intrinsically bursting neocortical pyramidal neurons. Neural Computation 6: 1086–1110.Google Scholar
  24. Ribary U, Ioannides AA, Singh KD, Hasson R, Bolton JPR, Lado F, Mogilner A, Llinás R (1991) Magnetic field tomography of coherent thalamocortical 40-Hz oscillations in humans. Proc. Natl. Acad. Sci. USA 88: 11037–11041.Google Scholar
  25. Rudy B (1988) Diversity and ubiquity of K channels. Neuroscience 25: 729–749.Google Scholar
  26. Sah P (1992) Model of IAHP. J. Neurophysiol. 28: 2237–2242.Google Scholar
  27. Sala F, Hernandez-Cruz A (1990) Calcium diffusion modeling in a spherical neuron. Biophys. J. 57: 313–324.Google Scholar
  28. Schiller J, Hemlchan F, Sakmann B (1995) Spatial profile of dendritic calcium transients evoked by action potentials in rat neocortical pyramidal neurones. J. Physiol. (Lond.) 487: 583–600Google Scholar
  29. Schiller J, Schiller Y, Stuart G, Sakmann B (1997) Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J. Physiol. (Lond.) 505: 605–616.Google Scholar
  30. Schwindt PC, Spain WJ, Foehring RC, Chubb MC, Crill WE (1988) Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes. J. Neurophysiol. 59: 450–467.Google Scholar
  31. Segev, I (1995) Cable and compartamental models of dendritic trees. In Bowen, J. (Ed.) The Book of Genesis, Springer, NY.Google Scholar
  32. Spruston N, Jaffe DB, Johnston D (1994) Dendritic attenuation of synaptic potentials and currents: The role of passive membrane properties. Trends Neurosci. 17: 161–166.Google Scholar
  33. Steriade M, Nunez A, Amzica F (1993) A novel slow (~1 Hz) oscillation of neocortical neurons in vivo: Depolarizing and hyperpolarizing components. J. Neuroscience 13(8): 3252–3265.Google Scholar
  34. Strowbridge and Tank (1994) Soc. Neurosci. Abst. 372: 12.Google Scholar
  35. Stuart GJ, Sakmann B (1994) Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367: 69–72.Google Scholar
  36. Traub RD, Wong RK, Miles R, Michelson H (1991) A model of a CA3 hippocampal pyramidal neuron incorporating voltageclamp data on intrinsic conductances. J. Neurophysiol. 66: 635–650.Google Scholar
  37. Westenbroek RE, Hell JW, Warner C, Dubel SJ, Snutch TP, Caterall WA (1992) Biochemical properties and subcellular distribution of an N-type calcium channel ®1 subunit. Neuron 9: 1099–1115.Google Scholar
  38. Yamada WM, Koch C, Adams PR (1989) Multiple channels and calcium dynamics. In: C Koch, I Segev, eds. Methods in Neuronal Modelling: From Synapses to Networks. MIT Press, Cambridge, MA. pp. 97–133.Google Scholar
  39. Yuste R, Gutnick MJ, Saar D, Delaney KD, Tank DW (1994) Calcium accumulations in dendrites from neocortical neurons: An apical band and evidence for functional compartments. Neuron 13: 23–43.Google Scholar
  40. Yuste R, Tank DW (1996) Dendritic integration in mammalian neurons, a century after Cajal. Neuron 16: 701–716.Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • Abdelkrim Elaagouby
    • 1
  • Rafael Yuste
    • 2
  1. 1.Division of BiologyCalifornia Institute of TechnologyPasadena
  2. 2.Department of Biological SciencesColumbia UniversityNew York

Personalised recommendations