Abstract
Recent experimental and theoretical studies have found that active dendritic ionic currents can compensate for the effects of electrotonic attenuation. In particular, temporal summation, the percentage increase in peak somatic voltage responses invoked by a synaptic input train, is independent of location of the synaptic input in hippocampal CA1 pyramidal neurons under normal conditions. This independence, known as normalization of temporal summation, is destroyed when the hyperpolarization-activated current, I h, is blocked [Magee JC (1999a), Nature Neurosci. 2: 508–514]. Using a compartmental model derived from morphological recordings of hippocampal CA1 pyramidal neurons, we examined the hypothesis that I h was primarily responsible for normalization of temporal summation. We concluded that this hypothesis was incomplete. With a model that included I h, the persistent Na+ current (I NaP), and the transient A-type K+ current (I A), however, we observed normalization of temporal summation across a wide range of synaptic input frequencies, in keeping with experimental observations.
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References
Andreasen M, Lambert JD (1999) Somatic amplification of distally generated subthreshold EPSPs in rat hippocampal pyramidal neurons. J. Physiol. 519: 85-100.
Berger T, Larkum ME, Luscher HR (2001) 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.
Buzsaki G, Turner DA (1998) Dendritic properties of hippocampal CA1 pyramidal neurons in the rat: Intracellular staining in vivo and in vitro. J. Comp. Neurol. 391: 335-352.
Cannon RC (1998a) cvapp: neuronal morphology viewer, editor and file converter. URL: http://www.cns.soton.ac.uk/~jchad/cellArchive/cellArchive.html.
Cannon RC, Turner DA, Pyapali GK, Wheal HV (1998b) An online archive of reconstructed hippocampal neurons. J. Neurosci. Methods 84: 49-54. URL: http://www.cns.soton.ac.uk/~jchad/ cellArchive/cellArchive.html.
Cook EP, Johnston D (1999) Voltage-dependent properties of dendrites that eliminate location-dependent variability of synaptic input. J. Neurophysiol. 81: 535-543.
De Schutter E, Bower JM (1994) An active membrane model of the cerebellar Purkinje cell I. Simulation of current clamps in slice. J. Neurophysiol. 71: 375-400.
French CR, Sah P, Buckett KJ, Gage PW (1990) Avoltage-dependent persistent sodium current in mammalian hippocampal neurons. J. Gen. Physiol. 95: 1139-1157.
Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput. 9: 1179-1209.
Hoffman DA, Magee JC, Colbert CM, Johnston D (1997) K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387: 869-875.
Holmes WR, Rall W (1992) Electrotonic length estimates in neurons with dendritic tapering or somatic shunt. J. Neurophysiol. 68: 1421-1437.
Huguenard JR, McCormick DA (1992) Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons. J. Neurophysiol. 68: 1373-1383.
Johnston D, Hoffman DA, Magee JC, Poolos NP, Watanabe S, Colbert CM, Migliore M (2000) Dendritic potassium channels in hippocampal pyramidal neurons. J. Physiol. 525(1): 75-81.
Johnston D, Magee JC, Colbert CM, Christie BR (1996) Active properties of neuronal dendrites. Ann. Rev. Neurosci. 19: 165-186.
Koch C (1999) Biophysics of computation: Information processing in single neurons. Oxford University Press, Oxford.
Lipowsky R, Gillessen T, Alzheimer C (1996) Dendritic Na+ channels amplify EPSPs in hippocampal CA1 pyramidal cells. J. Neurophysiol. 76: 2181-2191.
Magee JC (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J. Neurosci. 18: 7613-7624.
Magee JC (1999a) Dendritic Ih normalizes temporal summation in hippocampal CA1 neurons. Nature Neurosci. 2: 508-514.
Magee JC (1999b) Voltage-gated ion channels. In: G Stuart, N Spruston, M Hausser, eds. Dendrites. Oxford University Press, Oxford. pp. 139-160.
Magee JC, Johnston D (1995) Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268: 301-304.
Migliore M, Hoffman DA, Magee JC, Johnston (1999) Role of an Atype K+ conductance in the back-propagation of action potentials in the dendrites of hippocampal pyramidal neurons. J Comput. Neurosci. 7: 5-15.
Pape H-C (1996) Queer current and pacemaker: The hyperpolarization-activated cation current in neurons. Ann. Rev. Physiol. 58: 299-327.
Rapp M, Yarom Y, Segev I (1992) The impact of parallel fiber background activity on the cable properties of cerebellar Purkinje cells. Neural Comput. 4: 518-533.
Schwindt PC, Crill WE (1997) Modification of current transmitted from apical dendrite to soma by blockade of voltage-and Ca2+-dependent conductances in rat neocortical pyramidal neurons. J. Neurophysiol. 78: 187-198.
Segev I, London M (1999) A theoretical view of passive and active dendrites. In: G Stuart, N Spruston, M Hausser, eds. Dendrites. Oxford University Press, Oxford. pp. 205-230.
Segev I, London M (2000) Untangling dendrites with quantitative models. Science 290: 744-750.
Williams SR, Stuart GJ (2000) Site independence of EPSP time course is mediated by dendritic Ih in neocortical pyramidal neurons. J. Neurophysiol. 83: 3177-3182.
Yuste R, Tank DW (1996) Dendritic integration in mammalian neurons, a century after Cajal. Neuron 16: 701-716.
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Desjardins, A.E., Li, YX., Reinker, S. et al. The Influences of I h on Temporal Summation in Hippocampal CA1 Pyramidal Neurons: A Modeling Study. J Comput Neurosci 15, 131–142 (2003). https://doi.org/10.1023/A:1025881007453
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DOI: https://doi.org/10.1023/A:1025881007453