Anatomy and Functional Models of the Basal Ganglia

ABSTRACT

It has long been observed that diseases of the basal ganglia result in disorders of movement, both hypo- and hyperkinetic. An understanding of the anatomy, physiology, and neurochemistry of the component structures of the basal ganglia has greatly facilitated our understanding of control of movement in both health and disease. The direct-indirect pathway model developed in the late 1980s described two parallel channels of neuronal information converging to influence the output nuclei of the basal ganglia. According to this model, alterations in levels of excitation or inhibition produce changes in the absolute level of neuronal activity in the target structures and can be used to explain a number of observations from both laboratory and clinical settings. This model greatly aided our understanding of basal ganglia function and has contributed to the development of new therapies for movement disorders. However, there are a number of findings which are not satisfactorily explained, and a higher level of complexity of basal ganglia function is clearly implicated. Additional anatomically defined projections may serve as internal autoregulatory loops connecting external pathways. These are taken into account in a recently developed model and may help elucidate some of the contradictory evidence from both laboratory experiments and clinical results of neurosurgical interventions.

KEYWORD

Basal ganglia - models - movement disorders

REFERENCES

• 1 Kemp J M, Powell T PS. The structure of the caudate nucleus of the cat: light and electron microscopy.  Phil Trans R Soc Lond B . 1971;  262 383-401
• 2 Yelnik J, Francois C, Percheron G, Tande D. Morphological taxonomy of the neurons of the primate striatum.  J Comp Neurol . 1991;  31 273-294
• 3 Beach T G, McGeer E G. The distribution of substance P in the primate basal ganglia: an immunohistochemical study of the baboon and human brain.  Neuroscience . 1984;  13 29-52
• 4 Beckstead R M, Kersey K S. Immunohistochemical demonstration of differential substance P, met-enkephalin, and glutamic acid decarboxylase containing cell body and axon distributions in the corpus striatum of the cat.  J Comp Neurol . 1985;  232 481-498
• 5 Jessell T M, Emson P C, Paxinos G, Cuello A C. Topographic projections of substance P and GABA pathways in the striato- and pallido-nigral system: a biochemical and immunohistochemical study.  Brain Res . 1978;  152 487-498
• 6 Kanazawa I, Emson P C, Cuello A C. Evidence for the existence of substance P-containing fibres in the striato-nigral and pallido-nigral pathways in rat brain.  Brain Res . 1977;  119 447-453
• 7 Staines W A, Nagy J I, Vincent S R, Fibiger H C. Neurotransmitters contained in the efferents of the striatum.  Brain Res . 1980;  194 391-402
• 8 Besson M J, Graybiel A M, Quinn B. Co-expession of neuropeptides in the cat's striatum: an immunohistochemical study of substance P, dynorphin B and enkephalin.  Neuroscience . 1990;  39 33-58
• 9 Onn S P, Berger T W, Grace A A. Identification and characterization of striatal cell subtypes using in vivo intracellular recording and dye-labeling in rats, III: morphological correlates and compartmental localization.  Synapse . 1994;  16(3) 231-254
• 10 Gerfen C R, Engber T M, Mahan L C, Susel Z, Chase T N, Monsma Jr. J F. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons.  Science . 1990;  250 1429-1432
• 11 Aizman O, Brismar H, Uhlen P, Zettergren E, Levey A I, Forssberg H. Anatomical and physiological evidence for D1 and D2 dopamine receptor colocalization in neostriatal neurons.  Nat Neurosci . 2000;  3(3) 226-230
• 12 Nisenbaum E S, Grace A A, Berger T W. Functionally distinct subpopulations of striatal neurons are differentially regulated by GABAergic and dopaminergic inputs, II: in vitro analysis.  Neuroscience . 1992;  48(3) 579-593
• 13 Bolam J P, Izzo P N. The postsynaptic targets of substance P-immunoreactive terminals in the rat neostriatum with particular reference to identified spiny striatonigral neurons.  Exp Brain Res . 1988;  70 361-377
• 14 Haber S, Elde R P. Correlation between met-enkephalin and substance P immunoreactivity in the primate globus pallidus.  Neuroscience . 1981;  6 1291-1297
• 15 Hong J S, Yang H-YT, Racagni G, Costa E. Projections of substance P containing neurons from neostriatum to substantia nigra.  Brain Res . 1977;  122 541-544
• 16 Lee J-M, McLean S, Maggio J E, Zamir N, Roth R H, Eskay R L. The localization and characterization of substance P and substance K in striatonigral neurons.  Brain Res . 1986;  371 152-154
• 17 Bolam J P, Smith Y. The GABA and substance P input to dopaminergic neurones in the substantia nigra of the rat.  Brain Res . 1990;  529 57-78
• 18 Onn S P, Berger T W, Grace A A. Identification and characterization of striatal cell subtypes using in vivo intracellular recording in rats, II: membrane factors underlying paired-pulse response profiles.  Synapse . 1994;  16(3) 195-210
• 19 Bolam J P, Wainer B H, Smith A D. Characterization of cholinergic neurons in the rat neostriatum: a combination of choline acetyltransferase immunocytochemistry, Golgi-impregnation and electron microscopy.  Neuroscience . 1984;  12 711-718
• 20 Smith Y, Parent A. Neuropeptide Y-immunoreactive neurons in the striatum of cat and monkey: morphological characteristics, intrinsic organization and co-localization with somatostatin.  Brain Res . 1986;  372 241-252
• 21 Chesselet M-F, Graybiel A M. Striatal neurons expressing somatostatin-like immunoreactivity: evidence for a peptidergic interneuronal system in the cat.  Neuroscience . 1986;  17 547-571
• 22 Kubota Y, Mikawa S, Kawaguchi Y. Neostriatal GABAergic interneurones contain Nos, calretinin or parvalbumin.  Neuroreport . 1993;  5 205-208
• 23 Cowan R L, Wilson C J, Emson P C, Heizman C W. Parvalbumin-containing GABAergic interneurons in the rat neostriatum.  J Comp Neurol . 1990;  302 197-205
• 24 Smith A D, Bolam J P. The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurones.  Trends Neurosci . 1990;  13(7) 259-265
• 25 Freund T F, Powell J F, Smith A D. Tyrosine hydroxylase immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines.  Neuroscience . 1984;  13 1189-1215
• 26 Bouyer J J, Park D H, Joh T H, Pickel V M. Chemical and structural analysis of the relation between cortical inputs and tyrosine hydroxylase-containing terminals in rat neostriatum.  Brain Res . 1984;  302 267-275
• 27 Arbuthnott G W, Ingham C A, Wickens J R. Dopamine and synaptic plasticity in the neostriatum.  J Anat . 2000;  196(Pt 4) 587-596
• 28 Okubo Y, Suhara T, Sudo Y, Toru M. Possible role of dopamine D1 receptors in schizophrenia.  Mol Psychiatr . 1997;  2(4) 291-292
• 29 Calabresi P, Pisani A, Mercuri N B, Bernardi G. The corticostriatal projection: from synaptic plasticity to dysfunctions of the basal ganglia [see comments].  Trends Neurosci . 1996;  19(1) 19-24
• 30 Calabresi P, Centonze D, Bernardi G. Electrophysiology of dopamine in normal and denervated striatal neurons.  Trends Neurosci . 2000;  23(Suppl 10) S57-S63
• 31 Francois C, Percheron G, Parent A, Sadikot A F, Fenelon G, Yelnik J. Topography of the projection from the central complex of the thalamus to the sensorimotor striatal territory in monkeys.  J Comp Neurol . 1991;  305 17-34
• 32 Parent A, Mackey A, De Bellefeuille L. The subcortical afferents to caudate nucleus and putamen in primate: a fluorescence retrograde double labeling study.  Neuroscience . 1983;  10 1137-1150
• 33 Smith Y, Bennett B D, Bolam J P, Parent A, Sadikot A F. Synaptic relationships between dopaminergic afferents and cortical or thalamic input in the sensorimotor territory of the striatus in monkey.  J Comp Neurol . 1994;  344(1) 1-19
• 34 Sadikot A F, Parent A, Smith Y, Bolam J P. Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: a light and electron microscopic study of the thalamostriatal projection in relation to striatal heterogeneity.  J Comp Neurol . 1992;  320(2) 228-242
• 35 Graybiel A M, Ragsdale Jr W C. Histochemically distinct compartments in the striatum of human, monkey, and cat demonstrated by acetylthiocholinesterase staining.  Proc Natl Acad Sci USA . 1978;  75 5723-5726
• 36 Bolam J P, Izzo P N, Graybiel A M. Cellular substrates of the histochemically-defined striosome/matrix system of the caudate nucleus: a combined Golgi and immunocytochemical study in cat and ferret.  Neuroscience . 1988;  24 853-875
• 37 Izzo P N, Graybiel A M, Bolam J P. Characterization of substance P- and [Met]enkephalin- immunoreactive neurons in the caudate nucleus of cat and ferret by a single section Golgi procedure.  Neuroscience . 1987;  20 577-587
• 38 Graybiel A M, Ragsdale Jr W C, Yoneoka E S, Elde R P. An immunohistochemical study of enkephalins and other neuropeptides in the striatum of the cat with evidence that the peptides are arranged to form mosaic patterns in register with striosomal compartments visible by acetylcholinesterase staining.  Neuroscience . 1981;  6 377-397
• 39 Gerfen C R, Baimbridge K G, Miller J J. The neostriatal mosaic: compartmental distribution of calcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey.  Proc Natl Acad Sci USA . 1985;  82 8780-8784
• 40 Graybiel A M, Hirsch E C, Agid Y A. Differences in tyrosine hydroxylase-like immunoreactivity characterize the mesostriatal innervation of striosomes and extrastriosomal matrix at maturity.  Proc Natl Acad Sci USA . 1987;  84 303-307
• 41 Graybiel A M, Ragsdale Jr W C, Moon Edley S. Compartments in the striatum of the cat observed by retrograde cell-labelling.  Exp Brain Res . 1979;  34 189-195
• 42 Flaherty A W, Graybiel A M. Two input systems for body representations in the primate striatal matrix: experimental evidence in the squirrel monkey.  J Neurosci . 1993;  13(3) 1120-1137
• 43 Gimenez-Amaya J-M, Graybiel A M. Modular organization of projection neurons in the matrix compartment of the primate striatum.  J Neurosci . 1991;  11 779-791
• 44 Malach R, Graybiel A M. Mosaic architecture of the somatic sensory-recipient sector of the cat's striatum.  J Neurosci . 1986;  6 3436-3458
• 45 Ragsdale C W, Graybiel A M. Compartmental organization of the thalamostriatal connection in the cat.  J Comp Neurol . 1991;  134-167
• 46 Jimenez-Castellanos J, Graybiel A M. Evidence that histochemically distinct zones of the primate substantia nigra pars compacta are related to patterned distributions of nigrostriatal projection neurons and striatonigral fibers.  Exp Brain Res . 1989;  74 227-238
• 47 Ragsdale C W, Graybiel A M. The fronto-striatal projection in the cat and monkey and its relationship to inhomogeneities established by acetylcholinesterase histochemistry.  Brain Res . 1981;  208 259-266
• 48 Ragsdale Jr W C, Graybiel A M. Fibers from the basolateral nucleus of the amygdala selectively innervate striosomes in the caudate nucleus of the cat.  J Comp Neurol . 1988;  269 506-522
• 49 Walker R H, Graybiel A M. Dendritic arbors of spiny neurons in the primate striatum are directionally polarized.  J Comp Neurol . 1993;  337(4) 629-639
• 50 Walker R H, Arbuthnott G W, Baughman R W, Graybiel A M. Dendritic domains of medium spiny neurons in the primate striatum: relationships to striosomal borders.  J Comp Neurol . 1993;  337(4) 614-628
• 51 Francois C, Percheron G, Yelnik J, Heyner S. A Golgi analysis of the primate globus pallidus, I: inconstant processes of large neurons, other neuronal types, and afferent axons.  J Comp Neurol . 1984;  227 182-199
• 52 Robledo P, Feger J. Excitatory influence of rat subthalamic nucleus to substantia nigra pars reticulata and pallidal complex: electrophysiological data.  Brain Res . 1990;  528 47-54
• 53 Hamada I, DeLong M R. Lesions of the primate subthalamic nucleus (stn) reduce tonic and phasic neural activity in globus pallidus.  Soc Neurosci Abstr . 1988;  14 719
• 54 Yelnik J, Percheron G, François C. A golgi analysis of the primate globus pallidus, II: quantitative morphology and spatial orientation of dendritic arborizations.  J Comp Neurol . 1984;  227 200-213
• 55 Percheron G, Yelnik J, Francois C. A Golgi analysis of the primate globus pallidus, III: spatial organization of the striatopallidal complex.  J Comp Neurol . 1984;  227 214-227
• 56 van der Kooy D, Hattori T, Shannack K, Hornykiewicz O. The pallidosubthalamic projection in the rat: anatomical and biochemical studies.  Brain Res . 1981;  204 253-268
• 57 Hazrati L N, Parent A. Reciprocal connections between the two pallidal segments in primates.  Soc Neurosci Abstr . 1990;  16 1229
• 58 Smith Y, Bolam J P. Neurons of the substantia nigra reticulata receive a dense GABA-containing innervation from the globus pallidus in the rat.  Brain Res . 1989;  493 160-167
• 59 Walker R H, Arbuthnott G W, Wright A K. Electrophysiological and anatomical observations concerning the pallidostriatal pathway in the rat.  Exp Brain Res . 1989;  74 303-310
• 60 Parent A, Bouchard C, Smith Y. The striatopallidal and striatonigral projections: two distinct fiber systems in primate.  Brain Res . 1984;  303 385-390
• 61 Bevan M D, Clarke N P, Bolam J P. Synaptic integration of functionally diverse pallidal information in the entopeduncular nucleus and subthalamic nucleus in the rat.  J Neurosci . 1997;  17(1) 308-324
• 62 Bolam J P, Smith Y. The striatum and the globus pallidus send convergent synaptic inputs onto single cells in the entopeduncular nucleus of the rat: a double anterograde labelling study combined with postembedding immunocytochemistry for GABA.  J Comp Neurol . 1992;  321(3) 456-476
• 63 Smith Y, Lavoie B, Dumas J, Parent A. Evidence for a distinct nigropallidal dopaminergic projection in the squirrel monkey.  Brain Res . 1989;  482 381-386
• 64 Sidibe M, Bevan M D, Bolam J P, Smith Y. Efferent connections of the internal globus pallidus in the squirrel monkey, I: topography and synaptic organization of the pallidothalamic projection.  J Comp Neurol . 1997;  382(3) 323-347
• 65 Parent A, De Bellefeuille L. Organization of efferent projections from the internal segment of globus pallidus in primate as revealed by fluorescent retrograde labeling method.  Brain Res . 1982;  245 201-213
• 66 van der Kooy D, Carter D A. The organization of the efferent projections and striatal afferents of the entopeduncular nucleus and adjacent areas in the rat.  Brain Res . 1981;  211 15-36
• 67 Smith Y, Parent A. Neurons of the subthalamic nucleus in primates display glutamate but not GABA immunoreactivity.  Brain Res . 1988;  453 353-356
• 68 van der Kooy D, Hattori T. Single subthalamic nucleus neurons project to both the globus pallidus and substantia nigra in rat.  J Comp Neurol . 1980;  192 751-768
• 69 Smith Y, Hazrati L-N, Parent A. Efferent projections of the subthalamic nucleus in the squirrel monkey as studied by the PHA-L anterograde tracing method.  J Comp Neurol . 1990;  294 306-323
• 70 Bevan M D, Francis C M, Bolam J P. The glutamate-enriched cortical and thalamic input to neurons in the subthalamic nucleus of the rat: convergence with GABA-positive terminals.  J Comp Neurol . 1995;  361(3) 491-511
• 71 Hassani O K, Francois C, Yelnik J, Feger J. Evidence for a dopaminergic innervation of the subthalamic nucleus in the rat.  Brain Res . 1997;  749 88-94
• 72 van der Kooy D, Coscina D V, Hattori T. Is there a non-dopaminergic nigrostriatal pathway?.  Neuroscience . 1981;  6 345-357
• 73 Bentivoglio M, van der Kooy D, Kuypers H J M G. The organization of the efferent projections of the substantia nigra in the rat: a retrograde fluorescent double-labelling study.  Brain Res . 1979;  174 1-18
• 74 Lavoie B, Parent A. Pedunculopontine nucleus in the squirrel monkey: cholinergic and glutamatergic projections to the substantia nigra.  J Comp Neurol . 1994;  344 232-241
• 75 Smith Y, Bolam J P. The output neurones and the dopaminergic neurones of the substantia nigra receive a GABA-containing input from the globus pallidus in the rat.  J Comp Neurol . 1990;  296 47-64
• 76 Bevan M D, Smith A D, Bolam J P. The substantia nigra as a site of synaptic integration of functionally diverse information arising from the ventral pallidum and the globus pallidus in the rat.  Neuroscience . 1996;  75(1) 5-12
• 77 Smith Y, Bolam J P. Convergence of synaptic inputs from the striatum and globus pallidus onto identified nigrocollicular cells in the rat: a double anterograde labelling study.  Neuroscience . 1991;  44 45-74
• 78 Middleton F A, Strick P L. New concepts about the organization of basal ganglia output.  Adv Neurol . 1997;  74 57-68
• 79 Alexander G E, DeLong M R, Strick P L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex.  Annu Rev Neurosci . 1986;  9 357-381
• 80 Joel D, Weiner I. The organization of the basal ganglia-thalamocortical circuits: open interconnected rather than closed segregated.  Neuroscience . 1994;  63(2) 363-379
• 81 Obeso J A, Rodriguez-Oroz M C, Lanciego J L, Artieda J, Gonzalo N, Olanow C W. Pathophysiology of the basal ganglia in Parkinson's disease.  TINS . 2000;  23(Suppl 9) S8-S19
• 82 Albin R L, Young A B, Penney J B. The functional anatomy of basal ganglia disorders.  Trends Neurosci . 1989;  12 366-375
• 83 DeLong M R. Primate models of movement disorders of basal ganglia origin.  Trends Neurosci . 1990;  13 281-285
• 84 Bergman H, Wichmann T, DeLong M R. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus.  Science . 1990;  249 1436-1438
• 85 Wichmann T, Bergman H, DeLong M R. 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.  J Neurophysiol . 1994;  72(2) 521-530
• 86 Vitek J L, Zhang J, Evatt M, Mewes K, DeLong M R, Hashimoto T. GPi pallidotomy for dystonia: clinical outcome and neuronal activity.  Adv Neurol . 1998;  78 211-219
• 87 Hutchison W D, Lozano A M, Davis K D, Saint-Cyr J A, Lang A E, Dostrovsky J O. Differential neuronal activity in segments of globus pallidus in Parkinson's disease patients.  Neuroreport . 1994;  5 1533-1537
• 88 Lozano A M, Lang A E, Levy R, Hutchison W, Dostrovsky J. Neuronal recordings in Parkinson's disease patients with dyskinesias induced by apomorphine.  Ann Neurol . 2000;  47(4 Suppl 1) S141-S146
• 89 Hutchison W D, Levy R, Dostrovsky J O, Lozano A M, Lang A E. Effects of apomorphine on globus pallidus neurons in parkinsonian patients.  Ann Neurol . 1997;  42(5) 767-775
• 90 Davis K D, Taub E, Houle S, Lang A E, Dostrovsky J O, Tasker R R. Globus pallidus stimulation activates the cortical motor system during alleviation of parkinsonian symptoms [see comments].  Nat Med . 1997;  3(6) 671-674
• 91 Vitek J L, Chockkan V, Zhang J Y, Kaneoke Y, Evatt M, DeLong M R. Neuronal activity in the basal ganglia in patients with generalized dystonia and hemiballismus.  Ann Neurol . 1999;  46(1) 22-35
• 92 Lozano A M, Kumar R, Gross R E, Giladi N, Hutchison W D, Dostrovsky J O. Globus pallidus internus pallidotomy for generalized dystonia.  Movement Disord . 1997;  12(6) 865-870
• 93 Mitchell I J, Luquin R, Boyce S, Clarke C E, Robertson R G, Sambrook M A. Neural mechanisms of dystonia: evidence from a 2-deoxyglucose uptake study in a primate model of dopamine agonist-induced dystonia.  Mov Disord . 1990;  5 49-54
• 94 Crossman A R, Brotchie J M. Pathophysiology of dystonia.  Adv Neurol . 1998;  78 19-25
• 95 Ferrante R J, Kowall N W, Richardson Jr P E, Bird E D, Martin J B. Topography of enkephalin, substance P and acetylcholinesterase staining in Huntington's disease striatum.  Neurosci Lett . 1986;  71 283-288
• 96 Sapp E, Ge P, Aizawa H, Bird E, Penney J, Young A B. Evidence for a preferential loss of enkephalin immunoreactivity in the external globus pallidus in low grade Huntington's disease using high resolution image analysis.  Neuroscience . 1995;  64 397-404
• 97 Brotchie J M, Henry B, Hille C J, Crossman A R. Opioid peptide precursor expression in animal models of dystonia secondary to dopamine-replacement therapy in Parkinson's disease.  Adv Neurol . 1998;  78 41-52
• 98 Piccini P, Weeks R A, Brooks D J. Alterations in opioid receptor binding in Parkinson's disease patients with levodopa-induced dyskinesias.  Ann Neurol . 1997;  42(5) 720-726
• 99 Vila M, Levy R, Herrero M T, Faucheux B, Obeso J A, Agid Y. Metabolic activity of the basal ganglia in parkinsonian syndromes in human and non-human primates: a cytochrome oxidase histochemistry study.  Neuroscience . 1996;  71(4) 903-912
• 100 Herrero M T, Levy R, Ruberg M, Luquin M R, Villares J, Guillen J. Consequence of nigrostriatal denervation and L-dopa therapy on the expression of glutamic acid decarboxylase messenger RNA in the pallidum.  Neurology . 1996;  47(1) 219-224
• 101 Obeso J A, Rodriguez M C, Gorospe A, Guridi J, Alvarez L, Macias R. Surgical treatment of Parkinson's disease.  Baillieres Clin Neurol . 1997;  6(1) 125-145
• 102 Bhatia K P, Marsden C D. The behavioural and motor consequences of focal lesions of the basal ganglia in man.  Brain . 1994;  117 859-876
• 103 Missale C, Nash S R, Robinson S W, Jaber M, Caron M G. Dopamine receptors: from structure to function.  Physiol Rev . 1998;  78(1) 189-225
• 104 Hutchison W D, Lozano A M, Tasker R R, Lang A E, Dostrovsky J O. Identification and characterization of neurons with tremor-frequency activity in human globus pallidus.  Exp Brain Res . 1997;  113(3) 557-563
• 105 Schwarting R K, Huston J P. The unilateral 6-hydroxydopamine lesion model in behavioral brain research: analysis of functional deficits, recovery and treatments.  Prog Neurobiol . 1996;  50(2-3) 275-331
• 106 Kish L J, Palmer M R, Gerhardt G A. Multiple single-unit recordings in the striatum of freely moving animals: effects of apomorphine and D-amphetamine in normal and unilateral 6-hydroxydopamine-lesioned rats.  Brain Res . 1999;  833(1) 58-70
• 107 Onn S P, Grace A A. Alterations in electrophysiological activity and dye coupling of striatal spiny and aspiny neurons in dopamine-denervated rat striatum recorded in vivo.  Synapse . 1999;  33(1) 1-15
• 108 Onn S P, Grace A A. Dye coupling between rat striatal neurons recorded in vivo: compartmental organization and modulation by dopamine.  J Neurophysiol . 1994;  71(5) 1917-1934
• 109 Cepeda C, Walsh J P, Hull C D, Howard S G, Buchwald N A, Levine M S. Dye-coupling in the neostriatum of the rat, I: modulation by dopamine-depleting lesions.  Synapse . 1989;  4(3) 229-237
• 110 Onn S P, West A R, Grace A A. Dopamine-mediated regulation of striatal neuronal and network interactions.  Trends Neurosci . 2000;  23(Suppl 10) S48-S56
• 111 Arbuthnott G W, Ingham C A, Wickens J R. Dopamine and synaptic plasticity in the neostriatum.  J Anat . 2000;  196 (Pt 4) 587-596
• 112 Ingham C A, Hood S H, Taggart P, Arbuthnott G W. Plasticity of synapses in the rat neostriatum after unilateral lesion of the nigrostriatal dopaminergic pathway.  J Neurosci . 1998;  18(12) 4732-4743
• 113 Ingham C A, Hood S H, Van Maldegem B, Weenink A, Arbuthnott G W. Morphological changes in the rat neostriatum after unilateral 6-hydroxydopamine injections into the nigrostriatal pathway.  Exp Brain Res . 1993;  93(1) 17-27
• 114 Anglade P, Mouatt-Prigent A, Agid Y, Hirsch E. Synaptic plasticity in the caudate nucleus of patients with Parkinson's disease.  Neurodegeneration . 1996;  5(2) 121-128
• 115 Gillies A, Arbuthnott G. Computational models of the basal ganglia.  Mov Disord . 2000;  15(5) 762-770
• 116 Schultz W, Dickinson A. Neuronal coding of prediction errors.  Annu Rev Neurosci . 2000;  23 473-500
• 117 Redgrave P, Prescott T J, Gurney K. Is the short-latency dopamine response too short to signal reward error?.  Trends Neurosci . 1999;  22(4) 146-151
• 118 Kotter R, Wickens J. Striatal mechanisms in Parkinson's disease: new insights from computer modeling.  Artif Intell Med . 1998;  13(1-2) 37-55
• 119 Rutherford A, Garcia-Munoz M, Arbuthnott G W. An afterhyperpolarization recorded in striatal cells `in vitro': effect of dopamine administration.  Exp Brain Res . 1988;  71 399-405
• 120 Mink J W, Thach W T. Basal ganglia motor control, III: pallidal ablation: normal reaction time, muscle cocontraction, and slow movement.  J Neurophysiol . 1991;  65(2) 330-351
• 121 Kato M, Kimura M. Effects of reversible blockade of basal ganglia on a voluntary arm movement.  J Neurophysiol . 1992;  68(5) 1516-1534
• 122 Alamy M, Pons J C, Gambarelli D, Trouche E. A defective control of small-amplitude movements in monkeys with globus pallidus lesions: an experimental study on one component of pallidal bradykinesia.  Behav Brain Res . 1995;  72(1-2) 57-62
• 123 Mink J W, Thach W T. Basal ganglia motor control, I: nonexclusive relation of pallidal discharge to five movement modes.  J Neurophysiol . 1991;  65(2) 273-300
• 124 Bergman H, Feingold A, Nini A, Raz A, Slovin H, Abeles M. Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates.  Trends Neurosci . 1998;  21(1) 32-38