Autonomous pacemakers in the basal ganglia: who needs excitatory synapses anyway?

Autonomous pacemakers are crucial elements in many neural circuits. This is particularly true for the basal ganglia. This richly interconnected group of nuclei is rife with both fast- and slow-spiking pacemakers. Our understanding of the ionic mechanisms underlying pacemaking in these neurons is rapidly evolving, yielding new insights into the normal functioning of this network and how it goes awry in pathological states such as Parkinson's disease.

[1]  William A. Catterall,et al.  Neuromodulation of Na+ channels: An unexpected form of cellular platicity , 2001, Nature Reviews Neuroscience.

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

[3]  Charles J. Wilson,et al.  Regulation of the timing and pattern of action potential generation in rat subthalamic neurons in vitro by GABA-A IPSPs. , 2002, Journal of neurophysiology.

[4]  Nathan W. Gouwens,et al.  The Contribution of Resurgent Sodium Current to High-Frequency Firing in Purkinje Neurons: An Experimental and Modeling Study , 2003, The Journal of Neuroscience.

[5]  N. C. Harris,et al.  A possible pacemaker mechanism in pars compacta neurons of the guinea-pig substantia nigra revealed by various ion channel blocking agents , 1989, Neuroscience.

[6]  Jochen Roeper,et al.  Ih Channels Contribute to the Different Functional Properties of Identified Dopaminergic Subpopulations in the Midbrain , 2002, The Journal of Neuroscience.

[7]  G. Turrigiano Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same , 1999, Trends in Neurosciences.

[8]  A Kv3‐like persistent, outwardly rectifying, Cs+‐permeable, K+ current in rat subthalamic nucleus neurones , 2000, The Journal of physiology.

[9]  Alessandro Stefani,et al.  Effects of dihydropyridine calcium antagonists on rat midbrain dopaminergic neurones , 1994, British journal of pharmacology.

[10]  R. Harris-Warrick Voltage-sensitive ion channels in rhythmic motor systems , 2002, Current Opinion in Neurobiology.

[11]  B. Bean,et al.  Sodium currents in subthalamic nucleus neurons from Nav1.6-null mice. , 2004, Journal of neurophysiology.

[12]  G. Deuschl,et al.  Pathophysiology of Parkinson's disease: From clinical neurology to basic neuroscience and back , 2002, Movement disorders : official journal of the Movement Disorder Society.

[13]  N. Slater,et al.  Resurgent Na currents in four classes of neurons of the cerebellum. , 2004, Journal of neurophysiology.

[14]  B. Bean,et al.  Subthreshold Sodium Currents and Pacemaking of Subthalamic Neurons Modulation by Slow Inactivation , 2003, Neuron.

[15]  Bruce R. Johnson,et al.  Activity-Independent Homeostasis in Rhythmically Active Neurons , 2003, Neuron.

[16]  C. Sekirnjak,et al.  Long-Lasting Increases in Intrinsic Excitability Triggered by Inhibition , 2003, Neuron.

[17]  Dieter Jaeger,et al.  Sodium Channels and Dendritic Spike Initiation at Excitatory Synapses in Globus Pallidus Neurons , 2004, The Journal of Neuroscience.

[18]  I. Stanford,et al.  Electrophysiological and morphological characteristics of three subtypes of rat globus pallidus neurone in vitro , 2000, The Journal of physiology.

[19]  B. Bean,et al.  Subthreshold Sodium Current from Rapidly Inactivating Sodium Channels Drives Spontaneous Firing of Tuberomammillary Neurons , 2002, Neuron.

[20]  A. Grace,et al.  Intracellular and extracellular electrophysiology of nigral dopaminergic neurons—2. Action potential generating mechanisms and morphological correlates , 1983, Neuroscience.

[21]  D. James Surmeier,et al.  G-Protein-Coupled Receptor Modulation of Striatal CaV1.3 L-Type Ca Channels Is Dependent on a Shank-Binding Domain , 2005 .

[22]  Ivan Cohen,et al.  The Beat Goes On: Spontaneous Firing in Mammalian Neuronal Microcircuits , 2004, The Journal of Neuroscience.

[23]  D. Linden,et al.  Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons , 2000, Nature Neuroscience.

[24]  Pierre Pollak,et al.  Mechanisms of deep brain stimulation , 2002, Movement disorders : official journal of the Movement Disorder Society.

[25]  Weifeng Xu,et al.  Neuronal CaV1.3α1 L-Type Channels Activate at Relatively Hyperpolarized Membrane Potentials and Are Incompletely Inhibited by Dihydropyridines , 2001, The Journal of Neuroscience.

[26]  Nicolas Maurice,et al.  D2 Dopamine Receptor-Mediated Modulation of Voltage-Dependent Na+ Channels Reduces Autonomous Activity in Striatal Cholinergic Interneurons , 2004, The Journal of Neuroscience.

[27]  Jan-Marino Ramirez,et al.  Pacemaker neurons and neuronal networks: an integrative view , 2004, Current Opinion in Neurobiology.

[28]  P. Distefano,et al.  Sodium Channel β4, a New Disulfide-Linked Auxiliary Subunit with Similarity to β2 , 2003, The Journal of Neuroscience.

[29]  J. Tepper,et al.  Pallidal control of substantia nigra dopaminergic neuron firing pattern and its relation to extracellular neostriatal dopamine levels , 2004, Neuroscience.

[30]  I. Raman,et al.  Resurgent Sodium Current and Action Potential Formation in Dissociated Cerebellar Purkinje Neurons , 1997, The Journal of Neuroscience.

[31]  I. Engberg,et al.  Nifedipine‐ and omega‐conotoxin‐sensitive Ca2+ conductances in guinea‐pig substantia nigra pars compacta neurones. , 1993, The Journal of physiology.

[32]  William A Catterall,et al.  Transmitter Modulation of Slow, Activity-Dependent Alterations in Sodium Channel Availability Endows Neurons with a Novel Form of Cellular Plasticity , 2003, Neuron.

[33]  B. Amini,et al.  Calcium dynamics underlying pacemaker-like and burst firing oscillations in midbrain dopaminergic neurons: a computational study. , 1999, Journal of neurophysiology.

[34]  R. Palmiter,et al.  Dopamine controls the firing pattern of dopamine neurons via a network feedback mechanism , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Charles J. Wilson,et al.  Move to the rhythm: oscillations in the subthalamic nucleus–external globus pallidus network , 2002, Trends in Neurosciences.

[36]  Charles J. Wilson,et al.  Activity Patterns in a Model for the Subthalamopallidal Network of the Basal Ganglia , 2002, The Journal of Neuroscience.

[37]  A. Grace,et al.  Compensations after lesions of central dopaminergic neurons: some clinical and basic implications , 1990, Trends in Neurosciences.

[38]  David M. Smith,et al.  Firing properties of dopamine neurons in freely moving dopamine-deficient mice: effects of dopamine receptor activation and anesthesia. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[39]  T. Dawson,et al.  Molecular Pathways of Neurodegeneration in Parkinson's Disease , 2003, Science.

[40]  Jochen Roeper,et al.  Selective Coupling of T-Type Calcium Channels to SK Potassium Channels Prevents Intrinsic Bursting in Dopaminergic Midbrain Neurons , 2002, The Journal of Neuroscience.

[41]  Charles J. Wilson,et al.  Apamin-Sensitive Small Conductance Calcium-Activated Potassium Channels, through their Selective Coupling to Voltage-Gated Calcium Channels, Are Critical Determinants of the Precision, Pace, and Pattern of Action Potential Generation in Rat Subthalamic Nucleus Neurons In Vitro , 2003, The Journal of Neuroscience.

[42]  N. Mercuri,et al.  Intrinsic membrane properties and synaptic inputs regulating the firing activity of the dopamine neurons , 2002, Behavioural Brain Research.

[43]  B. Liss,et al.  Single‐cell mRNA expression of HCN1 correlates with a fast gating phenotype of hyperpolarization‐activated cyclic nucleotide‐gated ion channels (Ih) in central neurons , 2000, The European journal of neuroscience.

[44]  Keiichi Nagata,et al.  Kv3.4 subunits enhance the repolarizing efficiency of Kv3.1 channels in fast-spiking neurons , 2003, Nature Neuroscience.

[45]  D. Surmeier,et al.  Delayed Rectifier Currents in Rat Globus Pallidus Neurons Are Attributable to Kv2.1 and Kv3.1/3.2 K+ Channels , 1999, The Journal of Neuroscience.

[46]  J J Jack,et al.  Electrophysiology of dopaminergic and non‐dopaminergic neurones of the guinea‐pig substantia nigra pars compacta in vitro. , 1991, The Journal of physiology.

[47]  I. Raman,et al.  Open-Channel Block by the Cytoplasmic Tail of Sodium Channel β4 as a Mechanism for Resurgent Sodium Current , 2005, Neuron.

[48]  Bernardo Rudy,et al.  Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing , 2001, Trends in Neurosciences.

[49]  D James Surmeier,et al.  HCN2 and HCN1 Channels Govern the Regularity of Autonomous Pacemaking and Synaptic Resetting in Globus Pallidus Neurons , 2004, The Journal of Neuroscience.

[50]  D. Jaeger,et al.  Globus Pallidus Discharge Is Coincident with Striatal Activity during Global Slow Wave Activity in the Rat , 2003, The Journal of Neuroscience.

[51]  Daniel Padgett,et al.  Ionic Currents and Spontaneous Firing in Neurons Isolated from the Cerebellar Nuclei , 2000, The Journal of Neuroscience.

[52]  Ping Hx,et al.  Apamin-sensitive Ca2+-activated K+ channels regulate pacemaker activity in nigral dopamine neurons , 1996 .

[53]  Charles J. Wilson,et al.  Synaptic Regulation of Action Potential Timing in Neostriatal Cholinergic Interneurons , 1998, The Journal of Neuroscience.

[54]  Charles J. Wilson,et al.  The Mechanism of Intrinsic Amplification of Hyperpolarizations and Spontaneous Bursting in Striatal Cholinergic Interneurons , 2005, Neuron.

[55]  J. Wickens,et al.  Modulation of an Afterhyperpolarization by the Substantia Nigra Induces Pauses in the Tonic Firing of Striatal Cholinergic Interneurons , 2004, The Journal of Neuroscience.

[56]  A. Grace,et al.  Intracellular and extracellular electrophysiology of nigral dopaminergic neurons—1. Identification and characterization , 1983, Neuroscience.

[57]  M. Takada,et al.  Immunohistochemical localization of voltage‐gated calcium channels in substantia nigra dopamine neurons , 2001, The European journal of neuroscience.

[58]  B Bioulac,et al.  Slowly inactivating sodium current (I(NaP)) underlies single-spike activity in rat subthalamic neurons. , 2000, Journal of neurophysiology.

[59]  A M Graybiel,et al.  The basal ganglia and adaptive motor control. , 1994, Science.

[60]  I. Raman,et al.  Altered Subthreshold Sodium Currents and Disrupted Firing Patterns in Purkinje Neurons of Scn8a Mutant Mice , 1997, Neuron.

[61]  Jochen Roeper,et al.  Differential Expression of the Small-Conductance, Calcium-Activated Potassium Channel SK3 Is Critical for Pacemaker Control in Dopaminergic Midbrain Neurons , 2001, The Journal of Neuroscience.

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

[63]  D. German,et al.  Midbrain dopaminergic neurons in the mouse that contain calbindin-D28k exhibit reduced vulnerability to MPTP-induced neurodegeneration. , 1996, Neurodegeneration : a journal for neurodegenerative disorders, neuroprotection, and neuroregeneration.

[64]  C. Wilson,et al.  Coupled oscillator model of the dopaminergic neuron of the substantia nigra. , 2000, Journal of neurophysiology.