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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allbritton NL, Meyer T, Stryer L (1992) Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 258: 1812–1815.
Amitai Y, Friedman A, Connors BW, Gutnick MJ (1993) Regenerative activity in apical dendrites of pyramidal cells in neocortex. Cerebral Cortex 3: 26–38.
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.
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.
Connors BW, Gutnick MJ (1990) Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci. 13: 99–104.
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.
Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260: 3440–3450.
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.
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.
Johnston D, Wu SM-S (1995) Foundations of Cellular Neurophysiology. MIT Press, Cambridge, MA.
Kao JPY, Tsien RY (1988) Ca2+ binding kinetics of fura-2 and azo-1 from temperature-jum relaxation measurements. Biophys. J. 53: 635–639.
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.
Latorre R, Oberhauser A, Labarca P, Alvarez O (1989) Varieties of calcium-activated potassium channels. Ann. Rev. Physiol. 51: 385–399.
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.
Magee JC, Johnston D (1995) Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268: 301–304.
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.
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.
Pinsky PF, Rinzel J (1994) Intrinsic and network rhythmogenesis in a reduced Traub model for CA3 neurons. J. Comput. Neurosci. 1: 39–60.
Pockberger H (1991) Electrophysiological and morphological properties of rat motor cortex neurons in vivo. Brain Res. 539: 181–190.
Ramón y Cajal S (1904) La Textura del Sistema Nerviosa del Hombre y los Vertebrados. Moya, Madrid.
Regehr WG, Tank DW (1992) Calcium concentration dynamics produced by synaptic activation of CA1 hippocampal pyramidal cells. J. Neurosci. 12: 4202–4223.
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.
Rhodes PA, Gray CM (1994) Simulations of intrinsically bursting neocortical pyramidal neurons. Neural Computation 6: 1086–1110.
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.
Rudy B (1988) Diversity and ubiquity of K channels. Neuroscience 25: 729–749.
Sah P (1992) Model of IAHP. J. Neurophysiol. 28: 2237–2242.
Sala F, Hernandez-Cruz A (1990) Calcium diffusion modeling in a spherical neuron. Biophys. J. 57: 313–324.
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: 583–600
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.
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.
Segev, I (1995) Cable and compartamental models of dendritic trees. In Bowen, J. (Ed.) The Book of Genesis, Springer, NY.
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.
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.
Strowbridge and Tank (1994) Soc. Neurosci. Abst. 372: 12.
Stuart GJ, Sakmann B (1994) Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367: 69–72.
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.
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.
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.
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.
Yuste R, Tank DW (1996) Dendritic integration in mammalian neurons, a century after Cajal. Neuron 16: 701–716.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Elaagouby, A., Yuste, R. Role of Calcium Electrogenesis in Apical Dendrites: Generation of Intrinsic Oscillations by an Axial Current. J Comput Neurosci 7, 41–53 (1999). https://doi.org/10.1023/A:1008915510264
Issue Date:
DOI: https://doi.org/10.1023/A:1008915510264