Voltage‐dependent membrane potential oscillations of rat striatal fast‐spiking interneurons

We used whole‐cell recordings to investigate subthreshold membrane potential oscillations and their relationship with intermittent firing in striatal fast‐spiking interneurons. During current injections (100–500 pA, 1 s), these cells displayed a highly variable pattern of spike bursts (comprising 1–30 action potentials) interspersed with membrane potential oscillations. The oscillation threshold was −42 ± 10 mV, and coincided with that for action potentials. The oscillation frequency was voltage dependent and ranged between 20 and 100 Hz. Oscillations were unaffected by the calcium channel blockers cadmium and nickel and by blockers of ionotropic glutamate and GABA receptors. Conversely, the sodium channel blocker tetrodotoxin fully abolished the oscillations and the spike bursts. The first spike of a burst appeared to be triggered by an oscillation, since the timing and rate of rise of the membrane potential in the subthreshold voltage region was similar for the two events. Conversely, the second spike (and the subsequent ones) displayed much faster depolarisations in the subthreshold voltage range, indicating that they were generated by a different mechanism. Consistent with these notions, a small pulse of intracellular current delivered during the oscillation was effective in triggering a burst of action potentials that largely outlasted the pulse. We conclude that fast‐spiking interneuron oscillations are generated by an intrinsic membrane mechanism that does not require fast synaptic transmission, and which depends on sodium conductance but not calcium conductance, and that such oscillations are responsible for triggering the intermittent spike bursts that are typical of these neurons.

[1]  T Nagatsu,et al.  Synaptic integration mediated by striatal cholinergic interneurons in basal ganglia function. , 2000, Science.

[2]  Richard M. Eglen,et al.  Regulation of Na+ channel distribution in the nervous system , 2001, Trends in Neurosciences.

[3]  W. Crill,et al.  Persistent sodium current in mammalian central neurons. , 1996, Annual review of physiology.

[4]  Charles J. Wilson,et al.  Surround inhibition among projection neurons is weak or nonexistent in the rat neostriatum. , 1994, Journal of neurophysiology.

[5]  Hannah Monyer,et al.  Functional and Molecular Differences between Voltage-Gated K+ Channels of Fast-Spiking Interneurons and Pyramidal Neurons of Rat Hippocampus , 1998, The Journal of Neuroscience.

[6]  Jeffery R Wickens,et al.  Inhibitory interactions between spiny projection neurons in the rat striatum. , 2002, Journal of neurophysiology.

[7]  A G Hawkes,et al.  A note on correlations in single ion channel records , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[8]  D. Johnston,et al.  Axonal Action-Potential Initiation and Na+ Channel Densities in the Soma and Axon Initial Segment of Subicular Pyramidal Neurons , 1996, The Journal of Neuroscience.

[9]  R. North,et al.  Opioids excite dopamine neurons by hyperpolarization of local interneurons , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  P. Jonas,et al.  Functional differences in Na+ channel gating between fast‐spiking interneurones and principal neurones of rat hippocampus , 1997, The Journal of physiology.

[11]  Charles J. Wilson,et al.  Striatal interneurones: chemical, physiological and morphological characterization , 1995, Trends in Neurosciences.

[12]  J. Bolam,et al.  Synaptic organisation of the basal ganglia , 2000, Journal of anatomy.

[13]  Y. Kawaguchi,et al.  Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  J. Tepper,et al.  Inhibitory control of neostriatal projection neurons by GABAergic interneurons , 1999, Nature Neuroscience.

[15]  K. Tang,et al.  Dopamine-dependent synaptic plasticity in striatum during in vivo development. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[16]  T. W. Berger,et al.  Functionally distinct subpopulations of striatal neurons are differentially regulated by gabaergic and dopaminergic inputs—II. In vitro analysis , 1992, Neuroscience.

[17]  Charles J. Wilson,et al.  Intrinsic Membrane Properties Underlying Spontaneous Tonic Firing in Neostriatal Cholinergic Interneurons , 2000, The Journal of Neuroscience.

[18]  P. Greengard,et al.  Dopamine and cAMP-Regulated Phosphoprotein 32 kDa Controls Both Striatal Long-Term Depression and Long-Term Potentiation, Opposing Forms of Synaptic Plasticity , 2000, The Journal of Neuroscience.

[19]  Paolo Calabresi,et al.  Electrophysiology of dopamine in normal and denervated striatal neurons , 2000, Trends in Neurosciences.

[20]  R. Traub,et al.  Neuronal networks for induced ‘40 Hz’ rhythms , 1996, Trends in Neurosciences.

[21]  J. Vincent,et al.  Control of Action Potential Timing by Intrinsic Subthreshold Oscillations in Olfactory Bulb Output Neurons , 1999, The Journal of Neuroscience.

[22]  G. Boehmer,et al.  Subthreshold oscillation of the membrane potential in magnocellular neurones of the rat supraoptic nucleus , 2000, The Journal of physiology.

[23]  S. H. Chandler,et al.  Membrane Resonance and Subthreshold Membrane Oscillations in Mesencephalic V Neurons: Participants in Burst Generation , 2001, The Journal of Neuroscience.

[24]  T. Kita,et al.  Active membrane properties of rat neostriatal neurons in an in vitro slice preparation , 2004, Experimental Brain Research.

[25]  B. MacVicar,et al.  Cyclic Nucleotide-Gated Channels Contribute to the Cholinergic Plateau Potential in Hippocampal CA1 Pyramidal Neurons , 2001, The Journal of Neuroscience.

[26]  Idan Segev,et al.  Subthreshold oscillations and resonant frequency in guinea‐pig cortical neurons: physiology and modelling. , 1995, The Journal of physiology.

[27]  Enrico Bracci,et al.  Dopamine excites fast-spiking interneurons in the striatum. , 2002, Journal of neurophysiology.

[28]  T. W. Berger,et al.  Functionally distinct subpopulations of striatal neurons are differentially regulated by gabaergic and dopaminergic inputs—I. In vivo analysis , 1992, Neuroscience.

[29]  C. Wilson,et al.  Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  A. Alonso,et al.  Ionic mechanisms for the subthreshold oscillations and differential electroresponsiveness of medial entorhinal cortex layer II neurons. , 1993, Journal of neurophysiology.

[31]  R. Spehlmann The effects of acetylcholine and dopamine on the caudate nucleus depleted of biogenic amines. , 1975, Brain : a journal of neurology.

[32]  J. Tepper,et al.  Dual Cholinergic Control of Fast-Spiking Interneurons in the Neostriatum , 2002, The Journal of Neuroscience.

[33]  Y. Kubota,et al.  Dependence of GABAergic Synaptic Areas on the Interneuron Type and Target Size , 2000, The Journal of Neuroscience.

[34]  J. Bolam,et al.  Selective Innervation of Neostriatal Interneurons by a Subclass of Neuron in the Globus Pallidus of the Rat , 1998, The Journal of Neuroscience.

[35]  P. Calabresi,et al.  Permissive role of interneurons in corticostriatal synaptic plasticity , 1999, Brain Research Reviews.