Dendritic low-threshold Ca2+ channels in rat cerebellar Purkinje cells: Possible physiological implications

Low-voltage activated (LVA) Ca2+ currents have been characterized in a large variety of neurons including cerebellar Purkinje cells (PCs). This review summarizes and discusses the biophysical, pharmacological properties, as well as the molecular identity of LVA Ca2+ channels described in PCs in various experimental conditions. Putative functional roles for LVA Ca2+ currents include generation of low-threshold Ca2+ spikes (LTS) that underlie burst firing, promotion of intrinsic oscillatory behaviour, Ca2+ entry close to the resting membrane potential and synaptic potentiation. Based on our recent findings on cerebellar rat PCs in slice cultures, this review presents the major evidence demonstrating that LVA Ca2+ channels produce a dendritic initiated LTS with a regulated propagation to the soma. This new role for LVA Ca2+ channels is particularly important in determining firing patterns in PCs.

[1]  P. Reiner,et al.  Ca2+ channels: diversity of form and function , 1992, Current Opinion in Neurobiology.

[2]  P. Ince,et al.  The expression of neuronal voltage-dependent calcium channels in human cerebellum. , 1995, Brain research. Molecular brain research.

[3]  V. Bindokas,et al.  Characteristics of voltage sensitive calcium channels in dendrites of cultured rat cerebellar neurons , 1993, Neuropharmacology.

[4]  H. Markram,et al.  Calcium transients in dendrites of neocortical neurons evoked by single subthreshold excitatory postsynaptic potentials via low-voltage-activated calcium channels. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[5]  E. Sher,et al.  Distribution of the voltage‐dependent calcium channel α1G subunit mRNA and protein throughout the mature rat brain , 1999, The European journal of neuroscience.

[6]  T. Snutch,et al.  Biochemical properties and subcellular distribution of the neuronal class E calcium channel alpha 1 subunit , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  S. Vincent,et al.  Structure and functional expression of a member of the low voltage-activated calcium channel family. , 1993, Science.

[8]  G. Mennessier,et al.  Molecular and Functional Properties of the Human α1G Subunit That Forms T-type Calcium Channels* , 2000, The Journal of Biological Chemistry.

[9]  J. Bower,et al.  An active membrane model of the cerebellar Purkinje cell. I. Simulation of current clamps in slice. , 1994, Journal of neurophysiology.

[10]  F. Pouille,et al.  Dendro‐somatic distribution of calcium‐mediated electrogenesis in Purkinje cells from rat cerebellar slice cultures , 2000, The Journal of physiology.

[11]  Professor Dr. John C. Eccles,et al.  The Cerebellum as a Neuronal Machine , 1967, Springer Berlin Heidelberg.

[12]  M. Häusser,et al.  Initiation and spread of sodium action potentials in cerebellar purkinje cells , 1994, Neuron.

[13]  Matthew A. Wilson,et al.  GENESIS: A System for Simulating Neural Networks , 1988, NIPS.

[14]  Rodolfo Llinás,et al.  P-type calcium channels in the somata and dendrites of adult cerebellar purkinje cells , 1992, Neuron.

[15]  R. Tsien,et al.  Contrasting biophysical and pharmacological properties of T-type and R-type calcium channels , 1997, Neuropharmacology.

[16]  B. Bean,et al.  Mibefradil inhibition of T-type calcium channels in cerebellar purkinje neurons. , 1998, Molecular pharmacology.

[17]  J. Hell,et al.  Biochemical properties and subcellular distribution of an N-type calcium hannel α1 subunit , 1992, Neuron.

[18]  C. Lingle,et al.  Properties of Ba2+ currents arising from human α1E and α1Eβ3 constructs expressed in HEK293 cells: physiology, pharmacology, and comparison to native T-type Ba2+ currents , 1998, Neuropharmacology.

[19]  A. Yool,et al.  Developmental changes in calcium conductances contribute to the physiological maturation of cerebellar Purkinje neurons in culture , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  Shigeo Watanabe,et al.  Low-threshold potassium channels and a low-threshold calcium channel regulate Ca2+ spike firing in the dendrites of cerebellar Purkinje neurons: a modeling study , 2001, Brain Research.

[21]  P. Lory,et al.  Specific contribution of human T‐type calcium channel isotypes (α1G, α1H and α1I) to neuronal excitability , 2002 .

[22]  F. Pouille,et al.  Control of the propagation of dendritic low‐threshold Ca2+ spikes in Purkinje cells from rat cerebellar slice cultures , 2002, The Journal of physiology.

[23]  L. Fagni,et al.  Voltage-activated calcium channels in rat Purkinje cells maintained in culture , 1989, Pflügers Archiv.

[24]  R. Llinás,et al.  Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. , 1980, The Journal of physiology.

[25]  Michael E. Adams,et al.  P-type calcium channels in rat central and peripheral neurons , 1992, Neuron.

[26]  Calcium currents in rat cerebellar purkinje cells maintained in culture , 1989, Neuroscience.

[27]  D. Tank,et al.  Dendritic Integration in Mammalian Neurons, a Century after Cajal , 1996, Neuron.

[28]  P. Kostyuk Low-voltage activated calcium channels: achievements and problems , 1999, Neuroscience.

[29]  S. Hagiwara,et al.  Kinetics and distribution of voltage-gated Ca, Na and K channels on the somata of rat cerebellar Purkinje cells , 1989, Pflügers Archiv.

[30]  P. Hockberger,et al.  Analysis of spontaneous electrical activity in cerebellar Purkinje cells acutely isolated from postnatal rats. , 1997, Journal of neurobiology.

[31]  D. T. Yue,et al.  The α1E Calcium Channel Exhibits Permeation Properties Similar to Low-Voltage-Activated Calcium Channels , 1996, The Journal of Neuroscience.

[32]  Shigeo Watanabe,et al.  Differential roles of two types of voltage-gated Ca2+ channels in the dendrites of rat cerebellar Purkinje neurons , 1998, Brain Research.

[33]  B H Gähwiler,et al.  Low-Threshold Ca2+ Currents in Dendritic Recordings from Purkinje Cells in Rat Cerebellar Slice Cultures , 1997, The Journal of Neuroscience.

[34]  M. Joëls,et al.  Low-threshold calcium current in dendrites of the adult rat hippocampus , 1993, Neuroscience Letters.

[35]  P. Lory,et al.  Alternatively Spliced α1G (CaV3.1) Intracellular Loops Promote Specific T-Type Ca2+ Channel Gating Properties , 2001 .

[36]  J R Huguenard,et al.  Low-threshold calcium currents in central nervous system neurons. , 1996, Annual review of physiology.

[37]  Bruce P. Bean,et al.  Ionic Currents Underlying Spontaneous Action Potentials in Isolated Cerebellar Purkinje Neurons , 1999, The Journal of Neuroscience.

[38]  R. Llinás,et al.  Localization of P-type calcium channels in the central nervous system. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[39]  D. Johnston,et al.  Multiple Channel Types Contribute to the Low-Voltage-Activated Calcium Current in Hippocampal CA3 Pyramidal Neurons , 1996, The Journal of Neuroscience.

[40]  D. Johnston,et al.  Active properties of neuronal dendrites. , 1996, Annual review of neuroscience.

[41]  D. Pietrobon,et al.  α1E Subunits Form the Pore of Three Cerebellar R-Type Calcium Channels with Different Pharmacological and Permeation Properties , 2000, The Journal of Neuroscience.

[42]  N. Klugbauer,et al.  Regulation of the calcium channel α1G subunit by divalent cations and organic blockers , 2000, Neuropharmacology.

[43]  A. Destexhe,et al.  Dendritic Low-Threshold Calcium Currents in Thalamic Relay Cells , 1998, The Journal of Neuroscience.

[44]  D. Pietrobon,et al.  Functional Diversity of P-Type and R-Type Calcium Channels in Rat Cerebellar Neurons , 1996, The Journal of Neuroscience.

[45]  M. Adams,et al.  P-type calcium channels blocked by the spider toxin ω-Aga-IVA , 1992, Nature.

[46]  G. Wang,et al.  Selective peptide antagonist of the class E calcium channel from the venom of the tarantula Hysterocrates gigas. , 1998, Biochemistry.

[47]  Jung-Ha Lee,et al.  Molecular characterization of a neuronal low-voltage-activated T-type calcium channel , 1998, Nature.

[48]  Y. Zhang,et al.  Cloning and characterization of alpha1H from human heart, a member of the T-type Ca2+ channel gene family. , 1998, Circulation research.

[49]  F. Crépel,et al.  Inward rectification and low threshold calcium conductance in rat cerebellar Purkinje cells. An in vitro study. , 1986, The Journal of physiology.

[50]  M. Kaneda,et al.  Low-threshold calcium current in isolated Purkinje cell bodies of rat cerebellum. , 1990, Journal of neurophysiology.

[51]  P. Kostyuk,et al.  Two types of low‐voltage‐activated Ca2+ channels in neurones of rat laterodorsal thalamic nucleus. , 1997, The Journal of physiology.

[52]  Min Zhuo,et al.  Dendritic Ca2+ Channels Characterized by Recordings from Isolated Hippocampal Dendritic Segments , 1997, Neuron.

[53]  Edmund M. Talley,et al.  Differential Distribution of Three Members of a Gene Family Encoding Low Voltage-Activated (T-Type) Calcium Channels , 1999, The Journal of Neuroscience.

[54]  J. G. Netzeband,et al.  L-Type Calcium Channels Mediate Calcium Oscillations in Early Postnatal Purkinje Neurons , 2000, The Journal of Neuroscience.

[55]  L J Regan,et al.  Voltage-dependent calcium currents in Purkinje cells from rat cerebellar vermis , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  E. Perez-Reyes,et al.  Nickel block of three cloned T-type calcium channels: low concentrations selectively block alpha1H. , 1999, Biophysical journal.

[57]  D. Paré,et al.  Physiological properties of central amygdala neurons: species differences , 2002, The European journal of neuroscience.

[58]  T. Snutch,et al.  Nickel Block of a Family of Neuronal Calcium Channels: Subtype- and Subunit-Dependent Action at Multiple Sites , 1996, The Journal of Membrane Biology.

[59]  John A. Freeman,et al.  Dendritic Spikes and Their Inhibition in Alligator Purkinje Cells , 1968, Science.