Computational physiology of the neural networks of the primate globus pallidus: function and dysfunction

Neuroscience - Tập 198 - Trang 171-192 - 2011
J.A. Goldberg1, H. Bergman2
1Department of Physiology, Feinberg School of Medicine, Northwestern University, 303 East Chicago Avenue, Chicago, IL 60611, USA
2Department of Medical Neurobiology (Physiology) and the Edmond and Lily Safra Center for Brain Sciences, The Hebrew University, Jerusalem, Israel

Tài liệu tham khảo

Abeles, 1982 Abeles, 1982, Quantification, smoothing, and confidence limits for single-units' histograms, J Neurosci Methods, 5, 317, 10.1016/0165-0270(82)90002-4 Abeles, 1991 Adler, 2010, Neurons in both pallidal segments change their firing properties similarly prior to closure of the eyes, J Neurophysiol, 103, 346, 10.1152/jn.00765.2009 Aertsen, 1989, Dynamics of neuronal firing correlation: modulation of “effective connectivity”, J Neurophysiol, 61, 900, 10.1152/jn.1989.61.5.900 Albin, 1989, The functional anatomy of basal ganglia disorders, Trends Neurosci, 12, 366, 10.1016/0166-2236(89)90074-X Aldridge, 1980, Sensory-motor processing in the caudate nucleus and globus pallidus: a single-unit study in behaving primates, Can J Physiol Pharmacol, 58, 1192, 10.1139/y80-182 Alvarez, 2005, Bilateral subthalamotomy in Parkinson's disease: initial and long-term response, Brain, 128, 570, 10.1093/brain/awh397 Alvarez, 2009, Therapeutic efficacy of unilateral subthalamotomy in Parkinson's disease: results in 89 patients followed up to 36 months, J Neurol Neurosurg Psychiatry, 80, 979, 10.1136/jnnp.2008.154948 Anderson, 1978, Discharge patterns of basal ganglia neurons during active maintenance of postural stability and adjustment to chair tilt, Brain Res, 143, 325, 10.1016/0006-8993(78)90572-3 Anderson, 1987, An analysis of potentially converging inputs to the rostral ventral thalamic nuclei of the cat, Exp Brain Res, 68, 260, 10.1007/BF00248792 Anderson, 1985, Influence of the globus pallidus on arm movements in monkeys, J Neurophysiol, 54, 433, 10.1152/jn.1985.54.2.433 Anderson, 1991, A quantitative analysis of pallidal discharge during targeted reaching movement in the monkey, Exp Brain Res, 86, 623, 10.1007/BF00230536 Arkadir, 2002, False detection of dynamic changes in pallidal neuron interactions by the joint peri-stimulus histogram method, 181 Arkadir, 2004, Independent coding of movement direction and reward prediction by single pallidal neurons, J Neurosci, 24, 10047, 10.1523/JNEUROSCI.2583-04.2004 Averbeck, 2004, Coding and transmission of information by neural ensembles, Trends Neurosci, 27, 225, 10.1016/j.tins.2004.02.006 Aziz, 1991, Lesion of the subthalamic nucleus for the alleviation of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism in the primate, Mov Disord, 6, 288, 10.1002/mds.870060404 Ballard, 1985, Permanent human parkinsonism due to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP): seven cases, Neurology, 35, 949, 10.1212/WNL.35.7.949 Bar-Gad, 2003, Functional correlations between neighboring neurons in the primate globus pallidus are weak or nonexistent, J Neurosci, 23, 4012, 10.1523/JNEUROSCI.23-10-04012.2003 Bar-Gad, 2003, Information processing, dimensionality reduction and reinforcement learning in the basal ganglia, Prog Neurobiol, 71, 439, 10.1016/j.pneurobio.2003.12.001 Bar-Gad, 2001, The neuronal refractory period causes a short-term peak in the autocorrelation function, J Neurosci Methods, 104, 155, 10.1016/S0165-0270(00)00335-6 Bar-Gad, 2001, Failure in identification of overlapping spikes from multiple neuron activity causes artificial correlations, J Neurosci Methods, 107, 1, 10.1016/S0165-0270(01)00339-9 Basso, 2005, Activity of substantia nigra pars reticulata neurons during smooth pursuit eye movements in monkeys, Eur J Neurosci, 22, 448, 10.1111/j.1460-9568.2005.04215.x Baufreton, 2009, Sparse but selective and potent synaptic transmission from the globus pallidus to the subthalamic nucleus, J Neurophysiol, 102, 532, 10.1152/jn.00305.2009 Bayer, 2004, Eye position and memory saccade related responses in substantia nigra pars reticulata, Exp Brain Res, 154, 428, 10.1007/s00221-003-1735-7 Bengtson, 2000, Electrophysiological properties of cholinergic and noncholinergic neurons in the ventral pallidal region of the nucleus basalis in rat brain slices, J Neurophysiol, 83, 2649, 10.1152/jn.2000.83.5.2649 Ben-Shaul, 2001, Trial to trial variability in either stimulus or action causes apparent correlation and synchrony in neuronal activity, J Neurosci Methods, 111, 99, 10.1016/S0165-0270(01)00389-2 Bergman, 1998, Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates, Trends Neurosci, 21, 32, 10.1016/S0166-2236(97)01151-X Bergman, 1990, Reversal of experimental parkinsonism by lesions of the subthalamic nucleus, Science, 249, 1436, 10.1126/science.2402638 Bergman, 1994, The primate subthalamic nucleus, J Neurophysiol, 72, 507, 10.1152/jn.1994.72.2.507 Bevan, 1998, Selective innervation of neostriatal interneurons by a subclass of neuron in the globus pallidus of the rat, J Neurosci, 18, 9438, 10.1523/JNEUROSCI.18-22-09438.1998 Bolam, 2000, Synaptic organisation of the basal ganglia, J Anat, 196, 527, 10.1046/j.1469-7580.2000.19640527.x Boraud, 2000, Ratio of inhibited-to-activated pallidal neurons decreases dramatically during passive limb movement in the MPTP-treated monkey, J Neurophysiol, 83, 1760, 10.1152/jn.2000.83.3.1760 Boraud, 2001, Dopamine agonist-induced dyskinesias are correlated to both firing pattern and frequency alterations of pallidal neurones in the MPTP-treated monkey, Brain, 124, 546, 10.1093/brain/124.3.546 Boraud, 2002, From single extracellular unit recording in experimental and human Parkinsonism to the development of a functional concept of the role played by the basal ganglia in motor control, Prog Neurobiol, 66, 265, 10.1016/S0301-0082(01)00033-8 Braitenberg, 1991 Brody, 1999, Correlations without synchrony, Neural Comput, 11, 1537, 10.1162/089976699300016133 Brody, 1999, Disambiguating different covariation types, Neural Comput, 11, 1527, 10.1162/089976699300016124 Bromberg-Martin, 2010, A pallidus-habenula-dopamine pathway signals inferred stimulus values, J Neurophysiol, 104, 1068, 10.1152/jn.00158.2010 Bronfeld, 2010, Bicuculline-induced chorea manifests in focal rather than globalized abnormalities in the activation of the external and internal globus pallidus, J Neurophysiol, 104, 3261, 10.1152/jn.00093.2010 Brotchie, 1991, Motor function of the monkey globus pallidus, Brain, 114, 1667, 10.1093/brain/114.4.1667 Brotchie, 1991, Motor function of the monkey globus pallidus, Brain, 114, 1685, 10.1093/brain/114.4.1685 Bugaysen, 2010, Electrophysiological characteristics of globus pallidus neurons, PLoS ONE, 5, e12001, 10.1371/journal.pone.0012001 Buonomano, 1999, A neural network model of temporal code generation and position-invariant pattern recognition, Neural Comput, 11, 103, 10.1162/089976699300016836 Burns, 1983, A primate model of parkinsonism: selective destruction of dopaminergic neurons in the pars compacta of the substantia nigra by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine, Proc Natl Acad Sci U S A, 80, 4546, 10.1073/pnas.80.14.4546 Carpenter, 1981, Interconnections and organization of pallidal and subthalamic nucleus neurons in the monkey, J Comp Neurol, 197, 579, 10.1002/cne.901970404 Carpenter, 1981, Connections of the subthalamic nucleus in the monkey, Brain Res, 224, 1, 10.1016/0006-8993(81)91113-6 Chan, 2011, HCN channelopathy in external globus pallidus neurons in models of Parkinson's disease, Nat Neurosci, 14, 85, 10.1038/nn.2692 Chan, 2004, HCN2 and HCN1 channels govern the regularity of autonomous pacemaking and synaptic resetting in globus pallidus neurons, J Neurosci, 24, 9921, 10.1523/JNEUROSCI.2162-04.2004 Charara, 1994, Brainstem dopaminergic, cholinergic and serotoninergic afferents to the pallidum in the squirrel monkey, Brain Res, 640, 155, 10.1016/0006-8993(94)91870-8 Chevalier, 1985, Disinhibition as a basic process in the expression of striatal functions, Brain Res, 334, 215, 10.1016/0006-8993(85)90213-6 Churchland, 2011, Variance as a signature of neural computations during decision making, Neuron, 69, 818, 10.1016/j.neuron.2010.12.037 Churchland, 2010, Stimulus onset quenches neural variability: a widespread cortical phenomenon, Nat Neurosci, 13, 369, 10.1038/nn.2501 Coban, 2009, Comparison of unilateral pallidotomy and subthalamotomy findings in advanced idiopathic Parkinson's disease, Br J Neurosurg, 23, 23, 10.1080/02688690802507775 Cohen, 2011, Measuring and interpreting neuronal correlations, Nat Neurosci, 14, 811, 10.1038/nn.2842 Cools, 2011, Serotonin and dopamine: unifying affective, activational, and decision functions, Neuropsychopharmacology, 36, 98, 10.1038/npp.2010.121 Cooper, 2000, Electrophysiological and morphological characteristics of three subtypes of rat globus pallidus neurone in vitro, J Physiol, 527, 291, 10.1111/j.1469-7793.2000.t01-1-00291.x Cossette, 1999, Extrastriatal dopaminergic innervation of human basal ganglia, Neurosci Res, 34, 51, 10.1016/S0168-0102(99)00029-2 Davis, 1979, Chronic parkinsonism secondary to intravenous injection of meperidine analogues, Psychiatry Res, 1, 249, 10.1016/0165-1781(79)90006-4 de la Rocha, 2007, Correlation between neural spike trains increases with firing rate, Nature, 448, 802, 10.1038/nature06028 Degos, 2009, Chronic but not Acute dopaminergic transmission interruption promotes a progressive increase in cortical beta frequency synchronization: relationships to vigilance state and akinesia, Cereb Cortex, 19, 1616, 10.1093/cercor/bhn199 Deister, 2009, Calcium-activated SK channels influence voltage-gated ion channels to determine the precision of firing in globus pallidus neurons, J Neurosci, 29, 8452, 10.1523/JNEUROSCI.0576-09.2009 DeLong, 1971, Activity of pallidal neurons during movement, J Neurophysiol, 34, 414, 10.1152/jn.1971.34.3.414 DeLong, 1972, Activity of basal ganglia neurons during movement, Brain Res, 40, 127, 10.1016/0006-8993(72)90118-7 DeLong, 1985, Primate globus pallidus and subthalamic nucleus: functional organization, J Neurophysiol, 53, 530, 10.1152/jn.1985.53.2.530 DeLong, 1974, Relation of basal ganglia, cerebellum, and motor cortex units to ramp and ballistic limb movements, Brain Res, 71, 327, 10.1016/0006-8993(74)90975-5 Delwaide, 2000, Projections from basal ganglia to tegmentum: a subcortical route for explaining the pathophysiology of Parkinson's disease signs?, J Neurol, 247, II75, 10.1007/PL00007765 Deniau, 1985, Disinhibition as a basic process in the expression of striatal functions, Brain Res, 334, 227, 10.1016/0006-8993(85)90214-8 Diamantaras, 1996 Difiglia, 1982, A Golgi and ultrastructural study of the monkey globus pallidus, J Comp Neurol, 212, 53, 10.1002/cne.902120105 Difiglia, 1988, Synaptic organization of the globus pallidus, J Electron Microsc Tech, 10, 247, 10.1002/jemt.1060100304 Doyle, 2005, Levodopa-induced modulation of subthalamic beta oscillations during self-paced movements in patients with Parkinson's disease, Eur J Neurosci, 21, 1403, 10.1111/j.1460-9568.2005.03969.x Ecker, 2010, Decorrelated neuronal firing in cortical microcircuits, Science, 327, 584, 10.1126/science.1179867 Edgerton, 2010, Dendritic sodium channels regulate network integration in globus pallidus neurons: a modeling study, J Neurosci, 30, 15146, 10.1523/JNEUROSCI.2662-10.2010 Eggermont, 1990 Elias, 2007, Statistical properties of pauses of the high-frequency discharge neurons in the external segment of the globus pallidus, J Neurosci, 27, 2525, 10.1523/JNEUROSCI.4156-06.2007 Elias, 2008, Balance of increases and decreases in firing rate of the spontaneous activity of basal ganglia high-frequency discharge neurons, J Neurophysiol, 100, 3086, 10.1152/jn.90714.2008 Engel, 1991, Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat, Proc Natl Acad Sci U S A, 88, 6048, 10.1073/pnas.88.14.6048 Erez, 2011, Dispersed activity during passive movement in the globus pallidus of the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated primate, PLoS ONE, 6, e16293, 10.1371/journal.pone.0016293 Ermentrout, 1996, Type I membranes, phase resetting curves, and synchrony, Neural Comput, 8, 979, 10.1162/neco.1996.8.5.979 Ermentrout, 2001, Traveling electrical waves in cortex: insights from phase dynamics and speculation on a computational role, Neuron, 29, 33, 10.1016/S0896-6273(01)00178-7 Evarts, 1964, Temporal patterns of discharge of pyramidal tract neurons during sleep and waking in the monkey, J Neurophysiol, 27, 152, 10.1152/jn.1964.27.2.152 Evarts, 1966, Pyramidal tract activity associated with a conditioned hand movement in the monkey, J Neurophysiol, 29, 1011, 10.1152/jn.1966.29.6.1011 Filion, 1991, Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism, Brain Res, 547, 142 Filion, 1991, Effects of dopamine agonists on the spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism, Brain Res, 547, 152 Földiák, 1989, Adaptive network for optimal feature extraction, Proc Int Joint Conf Neural Netw, 1, 401, 10.1109/IJCNN.1989.118615 Földiák, 1990, Forming sparse representations by local anti-Hebbian learning, Biol Cybern, 64, 165, 10.1007/BF02331346 Fox, 1974, The primate globus pallidus: a golgi and electron microscopic study, J Hirnforsch, 15, 75 Francois, 1984, A Golgi analysis of the primate globus pallidus, J Comp Neurol, 227, 182 Francois, 2000, Dopaminergic innervation of the subthalamic nucleus in the normal state, in MPTP-treated monkeys, and in Parkinson's disease patients, J Comp Neurol, 425, 121, 10.1002/1096-9861(20000911)425:1<121::AID-CNE10>3.0.CO;2-G Galvan, 2005, GABAergic modulation of the activity of globus pallidus neurons in primates: in vivo analysis of the functions of GABA receptors and GABA transporters, J Neurophysiol, 94, 990, 10.1152/jn.00068.2005 Ganmor, 2011, Sparse low-order interaction network underlies a highly correlated and learnable neural population code, Proc Natl Acad Sci U S A, 108, 9679, 10.1073/pnas.1019641108 Gdowski, 2007, Signaling patterns of globus pallidus internal segment neurons during forearm rotation, Brain Res, 1155, 56, 10.1016/j.brainres.2007.04.028 Gdowski, 2001, Context dependency in the globus pallidus internal segment during targeted arm movements, J Neurophysiol, 85, 998, 10.1152/jn.2001.85.2.998 Georgopoulos, 1983, Relations between parameters of step-tracking movements and single cell discharge in the globus pallidus and subthalamic nucleus of the behaving monkey, J Neurosci, 3, 1586, 10.1523/JNEUROSCI.03-08-01586.1983 Gerfen, 1990, D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons, Science, 250, 1429, 10.1126/science.2147780 Goldberg, 2007, Response properties and synchronization of rhythmically firing dendritic neurons, J Neurophysiol, 97, 208, 10.1152/jn.00810.2006 Goldberg, 2003, Globus pallidus discharge is coincident with striatal activity during global slow wave activity in the rat, J Neurosci, 23, 10058, 10.1523/JNEUROSCI.23-31-10058.2003 Gourévitch, 2007, A simple indicator of nonstationarity of firing rate in spike trains, J Neurosci Methods, 163, 181, 10.1016/j.jneumeth.2007.02.021 Gray, 1989, Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties, Nature, 338, 334, 10.1038/338334a0 Günay, 2008, Channel density distributions explain spiking variability in the globus pallidus: a combined physiology and computer simulation database approach, J Neurosci, 28, 7476, 10.1523/JNEUROSCI.4198-07.2008 Haber, 2008, The cortico-basal ganglia integrative network: the role of the thalamus, Brain Res Bull, 78, 69, 10.1016/j.brainresbull.2008.09.013 Haber, 2010, The reward circuit: linking primate anatomy and human imaging, Neuropsychopharmacology, 35, 4, 10.1038/npp.2009.129 Haber, 1983, Ramifications of the globus pallidus in the rat as indicated by patterns of immunohistochemistry, Neuroscience, 9, 245, 10.1016/0306-4522(83)90291-9 Hamada, 1990, Activity of identified wrist-related pallidal neurons during step and ramp wrist movements in the monkey, J Neurophysiol, 64, 1892, 10.1152/jn.1990.64.6.1892 Handel, 1999, Quantitative analysis of substantia nigra pars reticulata activity during a visually guided saccade task, J Neurophysiol, 82, 3458, 10.1152/jn.1999.82.6.3458 Handel, 2000, Contextual modulation of substantia nigra pars reticulata neurons, J Neurophysiol, 83, 3042, 10.1152/jn.2000.83.5.3042 Hanson, 2004, Sodium channels and dendritic spike initiation at excitatory synapses in globus pallidus neurons, J Neurosci, 24, 329, 10.1523/JNEUROSCI.3937-03.2004 Hashimoto, 2006, Slow oscillatory activity of rat globus pallidus neurons in vitro, Eur J Neurosci, 23, 443, 10.1111/j.1460-9568.2005.04582.x Hazrati, 1992, Convergence of subthalamic and striatal efferents at pallidal level in primates: an anterograde double-labeling study with biocytin and PHA-L, Brain Res, 569, 336, 10.1016/0006-8993(92)90648-S Hazrati, 1992, The striatopallidal projection displays a high degree of anatomical specificity in the primate, Brain Res, 592, 213, 10.1016/0006-8993(92)91679-9 Hazrati, 1990, Evidence for interconnections between the two segments of the globus pallidus in primates: a PHA-L anterograde tracing study, Brain Res, 533, 171, 10.1016/0006-8993(90)91813-V Hazrati, 1990, Evidence for interconnections between the two segments of the globus pallidus in primates: a PHA-L anterograde tracing study, Brain Res, 533, 171, 10.1016/0006-8993(90)91813-V Heimer, 2002, Dopamine replacement therapy reverses abnormal synchronization of pallidal neurons in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine primate model of Parkinsonism, J Neurosci, 22, 7850, 10.1523/JNEUROSCI.22-18-07850.2002 Heimer, 2002, Dopamine replacement therapy reverses abnormal synchronization of pallidal neurons in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine primate model of Parkinsonism, J Neurosci, 22, 7850, 10.1523/JNEUROSCI.22-18-07850.2002 Heimer, 2006, Dopamine replacement therapy does not restore the full spectrum of normal pallidal activity in the 1-methyl-4-phenyl-1,2,3,6-tetra-hydropyridine primate model of Parkinsonism, J Neurosci, 26, 8101, 10.1523/JNEUROSCI.5140-05.2006 Hikosaka, 1983, Visual and oculomotor functions of monkey substantia nigra pars reticulata, J Neurophysiol, 49, 1230, 10.1152/jn.1983.49.5.1230 Hill, 2011, Quality metrics to accompany spike sorting of extracellular signals, J Neurosci, 31, 8699, 10.1523/JNEUROSCI.0971-11.2011 Hodgkin, 1948, The local electric changes associated with repetitive action in a non-medullated axon, J Physiol, 107, 165, 10.1113/jphysiol.1948.sp004260 Hutchinson, 1997, Effects of apomorphine on globus pallidus neurons in parkinsonian patients, Ann Neurol, 42, 767, 10.1002/ana.410420513 Iwahori, 1981, A Golgi study on the globus pallidus of the mouse, J Comp Neurol, 197, 29, 10.1002/cne.901970104 Iwahori, 1981, Entopeduncular nucleus of the cat: a Golgi study, Exp Neurol, 72, 654, 10.1016/0014-4886(81)90014-5 Izhikevich, 1999, Class 1 neural excitability, conventional synapses, weakly connected networks, and mathematical foundations of pulse-coupled models, IEEE Trans Neural Netw, 10, 499, 10.1109/72.761707 Izhikevich, 2007 Jaeger, 1993, Primate basal ganglia activity in a precued reaching task: preparation for movement, Exp Brain Res, 95, 51, 10.1007/BF00229653 Jaeger, 1995, Neuronal activity in the striatum and pallidum of primates related to the execution of externally cued reaching movements, Brain Res, 694, 111, 10.1016/0006-8993(95)00780-T Jan, 2000, Dopaminergic innervation of the pallidum in the normal state, in MPTP-treated monkeys and in parkinsonian patients, Eur J Neurosci, 12, 4525 Johnson, 2008, Quantifying the neural elements activated and inhibited by globus pallidus deep brain stimulation, J Neurophysiol, 100, 2549, 10.1152/jn.90372.2008 Joshua, 2009, Synchronization of midbrain dopaminergic neurons is enhanced by rewarding events, Neuron, 62, 695, 10.1016/j.neuron.2009.04.026 Joshua, 2009, Encoding of probabilistic rewarding and aversive events by pallidal and nigral neurons, J Neurophysiol, 101, 758, 10.1152/jn.90764.2008 Joshua, 2007, Quantifying the isolation quality of extracellularly recorded action potentials, J Neurosci Methods, 163, 267, 10.1016/j.jneumeth.2007.03.012 Kaneoke, 1996, Burst and oscillation as disparate neuronal properties, J Neurosci Methods, 68, 211, 10.1016/0165-0270(96)00081-7 Kim, 1976, Projections of the globus pallidus and adjacent structures: an autoradiographic study in the monkey, J Comp Neurol, 169, 263, 10.1002/cne.901690302 Kimura, 1976, Interneuronal connectivity between visual cortical neurones of the cat as studied by cross-correlation analysis of their impulse discharges, Brain Res, 118, 329, 10.1016/0006-8993(76)90720-4 Kincaid, 1998, Connectivity and convergence of single corticostriatal axons, J Neurosci, 18, 4722, 10.1523/JNEUROSCI.18-12-04722.1998 Kita, 1994, Parvalbumin-immunopositive neurons in rat globus pallidus: a light and electron microscopic study, Brain Res, 657, 31, 10.1016/0006-8993(94)90950-4 Kita, 1994, Physiology of two disynaptic pathways from the sensori-motor cortex to the basal ganglia output nuclei, 263 Kita, 2001, Neostriatal and globus pallidus stimulation induced inhibitory postsynaptic potentials in entopeduncular neurons in rat brain slice preparations, Neuroscience, 105, 871, 10.1016/S0306-4522(01)00231-7 Kita, 2007, Globus pallidus external segment, Prog Brain Res, 160, 111, 10.1016/S0079-6123(06)60007-1 Kita, 2001, Number, origins, and chemical types of rat pallidostriatal projection neurons, J Comp Neurol, 437, 438, 10.1002/cne.1294 Kita, 1991, Intracellular study of rat globus pallidus neurons: membrane properties and responses to neostriatal, subthalamic and nigral stimulation, Brain Res, 564, 296, 10.1016/0006-8993(91)91466-E Kita, 1994, The morphology of globus pallidus projection neurons in the rat: an intracellular staining study, Brain Res, 636, 308, 10.1016/0006-8993(94)91030-8 Kita, 1999, Monkey globus pallidus external segment neurons projecting to the neostriatum, Neuroreport, 10, 1467, 10.1097/00001756-199905140-00014 Kitai, 1981, Cortical inputs to the subthalamus: intracellular analysis, Brain Res, 214, 411, 10.1016/0006-8993(81)91204-X Kitai, 1987, Anatomy and physiology of the subthalamic nucleus: a driving force of the basal ganglia, 357 Kleiner-Fisman, 2010, Long-term effect of unilateral pallidotomy on levodopa-induced dyskinesia, Mov Disord, 25, 1496, 10.1002/mds.23155 Krüger, 1988, Multimicroelectrode investigation of monkey striate cortex: spike train correlations in the infragranular layers, J Neurophysiol, 60, 798, 10.1152/jn.1988.60.2.798 Kühn, 2005, The relationship between local field potential and neuronal discharge in the subthalamic nucleus of patients with Parkinson's disease, Exp Neurol, 194, 212, 10.1016/j.expneurol.2005.02.010 Kumar, 2010, Spiking activity propagation in neuronal networks: reconciling different perspectives on neural coding, Nat Rev Neurosci, 11, 615, 10.1038/nrn2886 Lago-Fernández, 2001, Connection topology dependence of synchronization of neural assemblies on class 1 and 2 excitability, Neural Netw, 14, 687, 10.1016/S0893-6080(01)00032-6 Langston, 1983, Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis, Science, 219, 979, 10.1126/science.6823561 Langston, 1984, A comparison of the acute and chronic effects of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine (MPTP)-induced parkinsonism in humans and the squirrel monkey, Neurology, 34, 268 Leblois, 2007, Late emergence of synchronized oscillatory activity in the pallidum during progressive Parkinsonism, Eur J Neurosci, 26, 1701, 10.1111/j.1460-9568.2007.05777.x Lee, 1998, Variability and correlated noise in the discharge of neurons in motor and parietal areas of the primate cortex, J Neurosci, 18, 1161, 10.1523/JNEUROSCI.18-03-01161.1998 Lee, 2007, Internal pallidal neuronal activity during mild drug-related dyskinesias in Parkinson's disease: decreased firing rates and altered firing patterns, J Neurophysiol, 97, 2627, 10.1152/jn.00443.2006 Lemon, 1984 Levy, 2002, Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson's disease, Brain, 125, 1196, 10.1093/brain/awf128 Levy, 2002, Synchronized neuronal discharge in the basal ganglia of parkinsonian patients is limited to oscillatory activity, J Neurosci, 22, 2855, 10.1523/JNEUROSCI.22-07-02855.2002 Mallet, 2008, Parkinsonian beta oscillations in the external globus pallidus and their relationship with subthalamic nucleus activity, J Neurosci, 28, 14245, 10.1523/JNEUROSCI.4199-08.2008 Mallet, 2008, Disrupted dopamine transmission and the emergence of exaggerated beta oscillations in subthalamic nucleus and cerebral cortex, J Neurosci, 28, 4795, 10.1523/JNEUROSCI.0123-08.2008 Matsumura, 1995, Activity of pallidal neurons in the monkey during dyskinesia induced by injection of bicuculline in the external pallidum, Neuroscience, 65, 59, 10.1016/0306-4522(94)00484-M Mercer, 2007, Nav16 sodium channels are critical to pacemaking and fast spiking in globus pallidus neurons, J Neurosci, 27, 13552, 10.1523/JNEUROSCI.3430-07.2007 Merello, 1999, Apomorphine induces changes in GPi spontaneous outflow in patients with Parkinson's disease, Mov Disord, 14, 45, 10.1002/1531-8257(199901)14:1<45::AID-MDS1009>3.0.CO;2-F Miller, 1987, Altered tonic activity of neurons in the globus pallidus and subthalamic nucleus in the primate MPTP model of parkinsonism, 415 Mink, 1996, The basal ganglia: focused selection and inhibition of competing motor programs, Prog Neurobiol, 50, 381, 10.1016/S0301-0082(96)00042-1 Mink, 1991, Basal ganglia motor control, J Neurophysiol, 65, 273, 10.1152/jn.1991.65.2.273 Mink, 1991, Basal ganglia motor control, J Neurophysiol, 65, 301, 10.1152/jn.1991.65.2.301 Mitchell, 1987, The primate globus pallidus: neuronal activity related to direction of movement, Exp Brain Res, 68, 491, 10.1007/BF00249793 Mitchell, 1987, The primate nucleus basalis of Meynert: neuronal activity related to a visuomotor tracking task, Exp Brain Res, 68, 506, 10.1007/BF00249794 Mitelman, 2011, Neighboring pallidal neurons do not exhibit more synchronous oscillations than remote ones in the mptp primate model of Parkinson's disease, Front Syst Neurosci, 5, 54, 10.3389/fnsys.2011.00054 Morris, 2005, Physiological studies of information processing in the normal and Parkinsonian basal ganglia: pallidal activity in Go/No-Go task and following MPTP treatment, Prog Brain Res, 147, 285 Mushiake, 1995, Pallidal neuron activity during sequential arm movements, J Neurophysiol, 74, 2754, 10.1152/jn.1995.74.6.2754 Nakanishi, 1990, Intracellular study of rat entopeduncular nucleus neurons in an in vitro slice preparation: electrical membrane properties, Brain Res, 527, 81, 10.1016/0006-8993(90)91063-M Nakanishi, 1991, Intracellular study of rat entopeduncular nucleus neurons in an in vitro slice preparation: response to subthalamic stimulation, Brain Res, 549, 285, 10.1016/0006-8993(91)90469-C Nambu, 2004, A new dynamic model of the cortico-basal ganglia loop, Prog Brain Res, 143, 461, 10.1016/S0079-6123(03)43043-4 Nambu, 2007, Globus pallidus internal segment, Prog Brain Res, 160, 135, 10.1016/S0079-6123(06)60008-3 Nambu, 1994, Electrophysiology of globus pallidus neurons in vitro, J Neurophysiol, 72, 1127, 10.1152/jn.1994.72.3.1127 Nambu, 1997, Morphology of globus pallidus neurons: its correlation with electrophysiology in guinea pig brain slices, J Comp Neurol, 377, 85, 10.1002/(SICI)1096-9861(19970106)377:1<85::AID-CNE8>3.0.CO;2-F Nauta, 1978, Efferent projections of the subthalamic nucleus: an autoradiographic study in monkey and cat, J Comp Neurol, 180, 1, 10.1002/cne.901800102 Nawrot, 2008, Measurement of variability dynamics in cortical spike trains, J Neurosci Methods, 169, 374, 10.1016/j.jneumeth.2007.10.013 Nevet, 2007, Lack of spike-count and spike-time correlations in the substantia nigra reticulata despite overlap of neural responses, J Neurophysiol, 98, 2232, 10.1152/jn.00190.2007 Nini, 1995, 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, J Neurophysiol, 74, 1800, 10.1152/jn.1995.74.4.1800 Niv, 2007, Tonic dopamine: opportunity costs and the control of response vigor, Psychopharmacology (Berl), 191, 507, 10.1007/s00213-006-0502-4 Obeso, 2009, What can man do without basal ganglia motor output?, Exp Neurol, 220, 283, 10.1016/j.expneurol.2009.08.030 Oja, 1991, Learning in nonlinear constrained hebbian networks, 381 Oorschot, 1996, Total number of neurons in the neostriatal, pallidal, subthalamic, and substantia nigral nuclei of the rat basal ganglia: a stereological study using the cavalieri and optical disector methods, J Comp Neurol, 366, 580, 10.1002/(SICI)1096-9861(19960318)366:4<580::AID-CNE3>3.0.CO;2-0 Oram, 1998, The “Ideal Homunculus”: decoding neural population signals, Trends Neurosci, 21, 259, 10.1016/S0166-2236(97)01216-2 Papa, 1999, Internal globus pallidus discharge is nearly suppressed during levodopa-induced dyskinesias, Ann Neurol, 46, 732, 10.1002/1531-8249(199911)46:5<732::AID-ANA8>3.0.CO;2-Q Parent, 1993, Anatomical aspects of information processing in primate basal ganglia, Trends Neurosci, 16, 111, 10.1016/0166-2236(93)90135-9 Parent, 2000, Organization of the basal ganglia: the importance of axonal collateralization, Trends Neurosci, 23, S20, 10.1016/S1471-1931(00)00022-7 Parush, 2011, Dopaminergic balance between reward maximization and policy complexity, Front Syst Neurosci, 5, 22, 10.3389/fnsys.2011.00022 Percheron, 1994, The basal ganglia related system of primates: defintion, description and informational analysis, 3 Percheron, 1984, A Golgi analysis of the primate globus pallidus, J Comp Neurol, 227, 214, 10.1002/cne.902270207 Perkel, 1967, Neuronal spike trains and stochastic point processes, Biophys J, 7, 419, 10.1016/S0006-3495(67)86597-4 Ponzi, 2010, Sequentially switching cell assemblies in random inhibitory networks of spiking neurons in the striatum, J Neurosci, 30, 5894, 10.1523/JNEUROSCI.5540-09.2010 Prensa, 2000, Dopaminergic innervation of human basal ganglia, J Chem Neuroanat, 20, 207, 10.1016/S0891-0618(00)00099-5 Prescott, 2008, Pyramidal neurons switch from integrators in vitro to resonators under in vivo-like conditions, J Neurophysiol, 100, 3030, 10.1152/jn.90634.2008 Rav-Acha, 2008, Pre- and postsynaptic serotoninergic excitation of globus pallidus neurons, J Neurophysiol, 100, 1053, 10.1152/jn.00845.2007 Rav-Acha, 2005, Dynamic and spatial features of the inhibitory pallidal GABAergic synapses, Neuroscience, 135, 791, 10.1016/j.neuroscience.2005.05.069 Raz, 1996, Neuronal synchronization of tonically active neurons in the striatum of normal and parkinsonian primates, J Neurophysiol, 76, 2083, 10.1152/jn.1996.76.3.2083 Raz, 2001, Activity of pallidal and striatal tonically active neurons is correlated in mptp-treated monkeys but not in normal monkeys, J Neurosci, 21, RC128, 10.1523/JNEUROSCI.21-03-j0006.2001 Raz, 2000, Firing patterns and correlations of spontaneous discharge of pallidal neurons in the normal and the tremulous 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine vervet model of Parkinsonism, J Neurosci, 20, 8559, 10.1523/JNEUROSCI.20-22-08559.2000 Redgrave, 2010, Interactions between the midbrain superior colliculus and the basal ganglia, Front Neuroanat, 4, 10.3389/fnana.2010.00132 Renart, 2010, The asynchronous state in cortical circuits, Science, 327, 587, 10.1126/science.1179850 Richardson, 1986, Nucleus basalis of Meynert neuronal activity during a delayed response task in monkey, Brain Res, 399, 364, 10.1016/0006-8993(86)91529-5 Ryan, 1991, The role of the subthalamic nucleus in the response of globus pallidus neurons to stimulation of the prelimbic and agranular frontal cortices in rats, Exp Brain Res, 86, 641, 10.1007/BF00230538 Sadek, 2007, A single-cell analysis of intrinsic connectivity in the rat globus pallidus, J Neurosci, 27, 6352, 10.1523/JNEUROSCI.0953-07.2007 Sato, 2000, Single-axon tracing study of neurons of the external segment of the globus pallidus in primate, J Comp Neurol, 417, 17, 10.1002/(SICI)1096-9861(20000131)417:1<17::AID-CNE2>3.0.CO;2-I Schneidman, 2006, Weak pairwise correlations imply strongly correlated network states in a neural population, Nature, 440, 1007, 10.1038/nature04701 Schultheiss, 2010, Phase response curve analysis of a full morphological globus pallidus neuron model reveals distinct perisomatic and dendritic modes of synaptic integration, J Neurosci, 30, 2767, 10.1523/JNEUROSCI.3959-09.2010 Schultz, 1997, A neural substrate of prediction and reward, Science, 275, 1593, 10.1126/science.275.5306.1593 Sharott, 2005, Dopamine depletion increases the power and coherence of beta-oscillations in the cerebral cortex and subthalamic nucleus of the awake rat, Eur J Neurosci, 21, 1413, 10.1111/j.1460-9568.2005.03973.x Shink, 1995, Differential synaptic innervation of neurons in the internal and external segments of the globus pallidus by the GABA- and glutamate-containing terminals in the squirrel monkey, J Comp Neurol, 358, 119, 10.1002/cne.903580108 Shink, 1995, Differential synaptic innervation of neurons in the internal and external segments of the globus pallidus by the GABA- and glutamate-containing terminals in the squirrel monkey, J Comp Neurol, 358, 119, 10.1002/cne.903580108 Silberstein, 2003, Patterning of globus pallidus local field potentials differs between Parkinson's disease and dystonia, Brain, 126, 2597, 10.1093/brain/awg267 Smith, 1998, Microcircuitry of the direct and indirect pathways of the basal ganglia, Neuroscience, 86, 353 Smith, 1990, Efferent projections of the subthalamic nucleus in the squirrel monkey as studied by the PHA-L anterograde tracing method, J Comp Neurol, 294, 306, 10.1002/cne.902940213 Smith, 1988, Neurons of the subthalamic nucleus in primates display glutamate but not GABA immunoreactivity, Brain Res, 453, 353, 10.1016/0006-8993(88)90177-1 Smith, 2009, The thalamostriatal systems: anatomical and functional organization in normal and parkinsonian states, Brain Res Bull, 78, 60, 10.1016/j.brainresbull.2008.08.015 Smith, 2004, The thalamostriatal system: a highly specific network of the basal ganglia circuitry, Trends Neurosci, 27, 520, 10.1016/j.tins.2004.07.004 Spooren, 1996, Ventral pallidostriatal pathway in the monkey: evidence for modulation of basal ganglia circuits, J Comp Neurol, 370, 295, 10.1002/(SICI)1096-9861(19960701)370:3<295::AID-CNE2>3.0.CO;2-# Stanford, 2003, Independent neuronal oscillators of the rat globus pallidus, J Neurophysiol, 89, 1713, 10.1152/jn.00864.2002 Strutt, 2009, Five-year follow-up of unilateral posteroventral pallidotomy in Parkinson's disease, Surg Neurol, 71, 551, 10.1016/j.surneu.2008.03.039 Surmeier, 2005, Autonomous pacemakers in the basal ganglia: who needs excitatory synapses anyway?, Curr Opin Neurobiol, 15, 312, 10.1016/j.conb.2005.05.007 Sutton, 1998 Tkacik, 2010, Optimal population coding by noisy spiking neurons, Proc Natl Acad Sci U S A, 107, 14419, 10.1073/pnas.1004906107 Turner, 1997, Pallidal discharge related to the kinematics of reaching movements in two dimensions, J Neurophysiol, 77, 1051, 10.1152/jn.1997.77.3.1051 Turner, 2005, Context-dependent modulation of movement-related discharge in the primate globus pallidus, J Neurosci, 25, 2965, 10.1523/JNEUROSCI.4036-04.2005 Turner, 2010, Basal ganglia contributions to motor control: a vigorous tutor, Curr Opin Neurobiol, 20, 704, 10.1016/j.conb.2010.08.022 Vaadia, 1995, Dynamics of neuronal interactions in monkey cortex in relation to behavioural events, Nature, 373, 515, 10.1038/373515a0 Weinberger, 2009, Increased gamma oscillatory activity in the subthalamic nucleus during tremor in Parkinson's disease patients, J Neurophysiol, 101, 789, 10.1152/jn.90837.2008 Weinberger, 2006, Beta oscillatory activity in the subthalamic nucleus and its relation to dopaminergic response in Parkinson's disease, J Neurophysiol, 96, 3248, 10.1152/jn.00697.2006 Wichmann, 1994, The primate subthalamic nucleus, J Neurophysiol, 72, 494, 10.1152/jn.1994.72.2.494 Wichmann, 1994, The primate subthalamic nucleus, J Neurophysiol, 72, 521, 10.1152/jn.1994.72.2.521 Wichmann, 2006, Neuronal firing before and after burst discharges in the monkey basal ganglia is predictably patterned in the normal state and altered in Parkinsonism, J Neurophysiol, 95, 2120, 10.1152/jn.01013.2005 Yasukawa, 2004, Rat intralaminar thalamic nuclei projections to the globus pallidus: a biotinylated dextran amine anterograde tracing study, J Comp Neurol, 471, 153, 10.1002/cne.20029 Yelnik, 2002, Functional anatomy of the basal ganglia, Mov Disord, 17, S15, 10.1002/mds.10138 Yelnik, 1996, A spatial and quantitative study of the striatopallidal connection in the monkey, Neuroreport, 7, 985, 10.1097/00001756-199604100-00006 Yelnik, 1984, A Golgi analysis of the primate globus pallidus, J Comp Neurol, 227, 200, 10.1002/cne.902270206 York, 2007, Short and long-term motor and cognitive outcome of staged bilateral pallidotomy: a retrospective analysis, Acta Neurochir (Wien), 149, 857, 10.1007/s00701-007-1242-x Zaidel, 2010, Subthalamic span of beta oscillations predicts deep brain stimulation efficacy for patients with Parkinson's disease, Brain, 133, 2007, 10.1093/brain/awq144 Zheng, 2002, Corticostriatal combinatorics: the implications of corticostriatal axonal arborizations, J Neurophysiol, 87, 1007, 10.1152/jn.00519.2001 Zohary, 1994, Correlated neuronal discharge rate and its implications for psychophysical performance [published erratum appears in Nature (1994) 371(6495):358], Nature, 370, 140, 10.1038/370140a0