Subthalamic nucleus: a clock inside basal ganglia?

Abstract Subthalamic nucleus (STN) neurons have a pivotal role in basal ganglia, as a result of their intrinsic membrane properties, connections within the circuit and glutamatergic nature. Their innate pacemaker activity, consisting of a single-spike tonic mode of discharge, is abolished in the case of hemiballism, profoundly disrupted in the Parkinsonian state and replaced by a regular bursting mode under treatment (high-frequency stimulation, HFS). We propose that control STN activity represents a clock, an internal measure of time allowing the correct automatic execution of learned movements and, in particular, the automatic switch from one movement to the next in a sequential motor pattern. STN neuronal activity would be able to reset the frequency of oscillations of motor thalamo–cortical loops, notably in the γ band.

[1]  F. Murakami,et al.  Excitatory postsynaptic potentials trigger a plateau potential in rat subthalamic neurons at hyperpolarized states. , 2001, Journal of neurophysiology.

[2]  G Chouvet,et al.  Unrelated course of subthalamic nucleus and globus pallidus neuronal activities across vigilance states in the rat , 2000, The European journal of neuroscience.

[3]  Carlos M. Magariños‐Ascone,et al.  Subthalamic neuron activity related to tremor and movement in Parkinson's disease , 2000, The European journal of neuroscience.

[4]  H. Bergman,et al.  The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. , 1994, Journal of neurophysiology.

[5]  K. Akert,et al.  Projections of the precentral motor cortex and other cortical areas of the frontal lobe to the subthalamic nucleus in the monkey , 1978, Experimental Brain Research.

[6]  T. Robbins,et al.  Effects of STN lesions on simple vs choice reaction time tasks in the rat: preserved motor readiness, but impaired response selection , 2001, The European journal of neuroscience.

[7]  Y. Smith,et al.  Microcircuitry of the direct and indirect pathways of the basal ganglia. , 1998, Neuroscience.

[8]  J. Rothwell,et al.  Cortical correlate of the Piper rhythm in humans. , 1998, Journal of neurophysiology.

[9]  R. Llinás,et al.  Electrophysiology of mammalian thalamic neurones in vitro , 1982, Nature.

[10]  D. Contreras,et al.  Synchronization of fast (30-40 Hz) spontaneous oscillations in intrathalamic and thalamocortical networks , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  G. Pfurtscheller,et al.  Human cortical 40 Hz rhythm is closely related to EMG rhythmicity , 1996, Neuroscience Letters.

[12]  Charles J. Wilson,et al.  The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  Christa Neuper,et al.  40-Hz oscillations during motor behavior in man , 1993, Neuroscience Letters.

[14]  E. Fetz,et al.  Oscillatory activity in sensorimotor cortex of awake monkeys: synchronization of local field potentials and relation to behavior. , 1996, Journal of neurophysiology.

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

[16]  A. Parent,et al.  Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidium in basal ganglia circuitry , 1995, Brain Research Reviews.

[17]  P Limousin-Dowsey,et al.  Subthalamic nucleus, sensorimotor cortex and muscle interrelationships in Parkinson's disease. , 2001, Brain : a journal of neurology.

[18]  J R WHITTIER,et al.  Analysis of choreoid hyperkinesia in the rhesus monkey. Surgical and pharmacological analysis of hyperkinesia resulting from lesions in the subthalamic nucleus ol luys , 1950, The Journal of comparative neurology.

[19]  C. Hammond,et al.  High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. , 2001, Journal of neurophysiology.

[20]  D. McCormick,et al.  Properties of a hyperpolarization‐activated cation current and its role in rhythmic oscillation in thalamic relay neurones. , 1990, The Journal of physiology.

[21]  E. Bézard,et al.  High frequency stimulation of the internal Globus Pallidus (GPi) simultaneously improves parkinsonian symptoms and reduces the firing frequency of GPi neurons in the MPTP-treated monkey , 1996, Neuroscience Letters.

[22]  Y Agid,et al.  Evolution of changes in neuronal activity in the subthalamic nucleus of rats with unilateral lesion of the substantia nigra assessed by metabolic and electrophysiological measurements , 2000, The European journal of neuroscience.

[23]  C. Hammond,et al.  Experimental hemiballism in the monkey produced by unilateral kainic acid lesion in corpus Luysii , 1979, Brain Research.

[24]  D. Contreras,et al.  Electrophysiological properties of intralaminar thalamocortical cells discharging rhythmic (≈40 HZ) spike-bursts at ≈1000 HZ during waking and rapid eye movement sleep , 1993, Neuroscience.

[25]  A. Davies,et al.  Intrinsic programmes of growth and survival in developing vertebrate neurons , 1994, Trends in Neurosciences.

[26]  R. Llinás,et al.  Voltage-dependent burst-to-tonic switching of thalamic cell activity: an in vitro study. , 1984, Archives italiennes de biologie.

[27]  C. Marsden The mysterious motor function of the basal ganglia , 1982, Neurology.

[28]  J. Dostrovsky,et al.  Effects of apomorphine on subthalamic nucleus and globus pallidus internus neurons in patients with Parkinson's disease. , 2001, Journal of neurophysiology.

[29]  Paul Krack,et al.  Intraoperative microrecordings of the subthalamic nucleus in Parkinson's disease , 2002, Movement disorders : official journal of the Movement Disorder Society.

[30]  J. Deniau,et al.  Electrophysiological demonstration of an excitatory subthalamonigral pathway in the rat , 1978, Brain Research.

[31]  A. Benabid,et al.  Intrasubthalamic injection of 6‐hydroxydopamine induces changes in the firing rate and pattern of subthalamic nucleus neurons in the rat , 2001, Synapse.

[32]  O. Hassani,et al.  Increased subthalamic neuronal activity after nigral dopaminergic lesion independent of disinhibition via the globus pallidus , 1996, Neuroscience.

[33]  W. Schultz,et al.  Neuronal activity in monkey striatum related to the expectation of predictable environmental events. , 1992, Journal of neurophysiology.

[34]  G. Pfurtscheller Central beta rhythm during sensorimotor activities in man. , 1981, Electroencephalography and clinical neurophysiology.

[35]  Charles J. Wilson,et al.  Membrane potential synchrony of simultaneously recorded striatal spiny neurons in vivo , 1998, Nature.

[36]  E. Scarnati,et al.  Pharmacological study of the cortical-induced excitation of subthalamic nucleus neurons in the rat: Evidence for amino acids as putative neurotransmitters , 1987, Neuroscience.

[37]  V. Brown,et al.  Reaction time performance following unilateral striatal dopamine depletion and lesions of the subthalamic nucleus in the rat , 1999, The European journal of neuroscience.

[38]  J. Deniau,et al.  Relationships between the Prefrontal Cortex and the Basal Ganglia in the Rat: Physiology of the Corticosubthalamic Circuits , 1998, The Journal of Neuroscience.

[39]  T. Sejnowski,et al.  Thalamocortical oscillations in the sleeping and aroused brain. , 1993, Science.

[40]  K Watanabe,et al.  Neural information transferred from the putamen to the globus pallidus during learned movement in the monkey. , 1996, Journal of neurophysiology.

[41]  M. Mouroux,et al.  Evidence that the parafascicular projection to the subthalamic nucleus is glutamatergic. , 1993, Neuroreport.

[42]  J. Walters,et al.  The Response of Subthalamic Nucleus Neurons to Dopamine Receptor Stimulation in a Rodent Model of Parkinson’s Disease , 1997, The Journal of Neuroscience.

[43]  C. Marsden,et al.  Bradykinesia and impairment of EEG desynchronization in Parkinson's disease , 1999, Movement disorders : official journal of the Movement Disorder Society.

[44]  C. Wilson,et al.  Mechanisms Underlying Spontaneous Oscillation and Rhythmic Firing in Rat Subthalamic Neurons , 1999, The Journal of Neuroscience.

[45]  D. McCormick,et al.  Cellular mechanisms of a synchronized oscillation in the thalamus. , 1993, Science.

[46]  Abdelhamid Benazzouz,et al.  Time-course of changes in firing rates and firing patterns of subthalamic nucleus neuronal activity after 6-OHDA-induced dopamine depletion in rats , 2001, Brain Research.

[47]  O. Hassani,et al.  Effects of intrasubthalamic injection of dopamine receptor agonists on subthalamic neurons in normal and 6-hydroxydopamine-lesioned rats: an electrophysiological and c-Fos study , 1999, Neuroscience.

[48]  Okihide Hikosaka,et al.  Visual and oculomotor functions of monkey subthalamic nucleus. , 1992 .

[49]  J. Dostrovsky,et al.  Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson's disease. , 2002, Brain : a journal of neurology.

[50]  T. Robbins,et al.  Bilateral Lesions of the Subthalamic Nucleus Induce Multiple Deficits in an Attentional Task in Rats , 1997, The European journal of neuroscience.

[51]  F. Windels,et al.  Effects of high frequency stimulation of subthalamic nucleus on extracellular glutamate and GABA in substantia nigra and globus pallidus in the normal rat , 2000, The European journal of neuroscience.

[52]  J. Féger,et al.  Responses of subthalamic and pallidal neurons to striatal stimulation: an extracellular study on awake monkeys , 1976, Brain Research.

[53]  J.Purdon Martin A Contribution TO THE STUDY OF CHOREA.: THE SYMPTOMS WHICH RESULT FROM INJURY OF THE CORPUS LUYSII , 1928 .

[54]  J. Dostrovsky,et al.  Microelectrode recording-guided posteroventral pallidotomy in patients with Parkinson's disease. , 1997, Advances in neurology.

[55]  F. Chéruel,et al.  Activity of neurons of the subthalamic nucleus in relation to motor performance in the cat , 1996, Experimental Brain Research.

[56]  H. Bergman,et al.  The primate subthalamic nucleus. I. Functional properties in intact animals. , 1994, Journal of neurophysiology.

[57]  M R DeLong,et al.  The primate subthalamic nucleus. III. Changes in motor behavior and neuronal activity in the internal pallidum induced by subthalamic inactivation in the MPTP model of parkinsonism. , 1994, Journal of neurophysiology.

[58]  E. Fetz,et al.  Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[59]  T. Baumann,et al.  Tremor control after pallidotomy in patients with Parkinson's disease: correlation with microrecording findings. , 1997, Neurosurgical focus.

[60]  J. Deniau,et al.  Cortical inputs to the subthalamus: intracellular analysis , 1981, Brain Research.

[61]  O. Ottersen,et al.  Terminals of subthalamonigral fibres are enriched with glutamate-like immunoreactivity: An electron microscopic, immunogold analysis in the cat , 1993, Journal of Chemical Neuroanatomy.

[62]  A. Parent,et al.  Pedunculopontine nucleus in the squirrel monkey: Distribution of cholinergic and monoaminergic neurons in the mesopontine tegmentum with evidence for the presence of glutamate in cholinergic neurons , 1994, The Journal of comparative neurology.

[63]  K. D. Singh,et al.  Magnetic field tomography of coherent thalamocortical 40-Hz oscillations in humans. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[64]  D. Plenz,et al.  A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus , 1999, Nature.

[65]  A. Oliviero,et al.  Dopamine Dependency of Oscillations between Subthalamic Nucleus and Pallidum in Parkinson's Disease , 2001, The Journal of Neuroscience.

[66]  A. E. Lang,et al.  Identification and characterization of neurons with tremor-frequency activity in human globus pallidus , 1997, Experimental Brain Research.

[67]  B Bioulac,et al.  Activation of GABA(A) receptors in subthalamic neurons in vitro: properties of native receptors and inhibition mechanisms. , 2001, Journal of neurophysiology.

[68]  J. Hollerman,et al.  Subthalamic nucleus cell firing in the 6-OHDA-treated rat: basal activity and response to haloperidol , 1992, Brain Research.

[69]  M. D. Crutcher,et al.  Relations between parameters of step-tracking movements and single cell discharge in the globus pallidus and subthalamic nucleus of the behaving monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[70]  F. Murakami,et al.  Characterization of Ca(2+) channels in rat subthalamic nucleus neurons. , 2000, Journal of neurophysiology.

[71]  E. C. Hirsch,et al.  Metabolic activity of excitatory parafascicular and pedunculopontine inputs to the subthalamic nucleus in a rat model of Parkinson's disease , 2000, Neuroscience.

[72]  J. Dostrovsky,et al.  High-frequency Synchronization of Neuronal Activity in the Subthalamic Nucleus of Parkinsonian Patients with Limb Tremor , 2000, The Journal of Neuroscience.

[73]  H. Bergman,et al.  Neurons in the globus pallidus do not show correlated activity in the normal monkey, but phase-locked oscillations appear in the MPTP model of parkinsonism. , 1995, Journal of neurophysiology.

[74]  B Bioulac,et al.  Subthalamic Nucleus Neurons Switch from Single-Spike Activity to Burst-Firing Mode , 1999, The Journal of Neuroscience.

[75]  C. Hammond,et al.  Anatomical and electrophysiological studies on the reciprocal projections between the subthalamic nucleus and nucleus tegmenti pedunculopontinus in the rat , 1983, Neuroscience.

[76]  A. Morel,et al.  Single-unit analysis of the pallidum, thalamus and subthalamic nucleus in parkinsonian patients , 2000, Neuroscience.

[77]  Daniel Jeanmonod,et al.  Thalamocortical dysrhythmia II.: Clinical and surgical aspects , 2001 .

[78]  R. J. Allan,et al.  Neurophysiological identification of the subthalamic nucleus in surgery for Parkinson's disease , 1998, Annals of neurology.

[79]  R. Llinás,et al.  Thalamocortical dysrhythmia: A neurological and neuropsychiatric syndrome characterized by magnetoencephalography. , 1999, Proceedings of the National Academy of Sciences of the United States of America.