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Motor Functions of the Basal Ganglia

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Abstract

The sections in this article are:

1 Anatomical Background
1.1 Striatum
1.2 Pallidal‐Subthalamic Relations
1.3 Basal Ganglia Output
1.4 Thalamocortical Projections
2 Motor Effects of Lesions
2.1 General Considerations
2.2 Lesions of Individual Nuclei
3 Motor Effects of Electrical Stimulation
3.1 Electrical Stimulation in Alert Animals
3.2 Electrical Stimulation in Anesthetized Animals
3.3 Do Basal Ganglia Exert Inhibitory Influence on Motor Mechanisms?
4 Single‐Cell Studies in The Basal Ganglia
4.1 Spontaneous Activity
4.2 Temporal Relation to Movement
4.3 Somatotopic Organization
4.4 Relations to Parameters of Movement
4.5 Vestibular and Postural Mechanisms
4.6 Responses to Peripheral Stimuli
4.7 Relations to Specific Behaviors
4.8 Summary
5 Lesioning and Recording in Human Subjects
6 Motor Behavioral Studies
6.1 Reaction Time
6.2 Speed of Movement
6.3 Other Aspects of Motor Performance
6.4 Continuous Pursuit Movements
7 Pathophysiological Mechanisms of Basal Ganglia Disorders
7.1 Akinesia and Hyperactivity
7.2 Dyskinesias and Stereotyped Behavior
7.3 Rigidity
7.4 Resting Tremor
8 Interpretative Summary
Figure 1. Figure 1.

Schematic diagram of principal intrinsic and extrinsic connections of basal ganglia. GPe, external pallidal segment; GPi, internal pallidal segment; SNpr, substantia nigra pars reticulata; SNpc, substantia nigra pars compacta; STN, subthalamic nucleus; CM, center median; VL, n. ventralis lateralis; VA, n. ventralis anterior; SC, superior colliculus; RF, reticular formation; VTA, ventral tegmental area; TPC, n. tegmenti pedunculopontinus pars compacta. The dashed lines indicate dopamine pathways. Projections from the raphe to the striatum and substantia nigra have been omitted.

Figure 2. Figure 2.

Typical patterns of discharge observed during rest. GPe, external segment of globus pallidus; GPi, internal segment of globus pallidus; BORDER, “border” cells; S.I., substantia innominate cells. Cells in GPe fell into two groups: A: high‐frequency discharge neurons with recurrent long intervals and silence; and B: low‐frequency discharge bursting neurons. In contrast to GPe, cells in GPi (C) discharged in a continuous manner. Cells located along borders of the two pallidal segments (D) exhibited a fourth discharge pattern, similar to that of neurons in the substantia innominata (E).

From DeLong 60
Figure 3. Figure 3.

Activity of a high‐frequency discharge cell in external pallidal segment with monkey resting, during push‐pull (P‐P) and side‐to‐side (S‐S) movements of contralateral arm, and during push‐pull and side‐to‐side movements of ipsilateral arm. Line below unit represents position of rod. For push‐pull movements, up is for pull and down is for push; for side‐to‐side movements, up is for extension and down is for flexion. Discharge of this cell is phasically related to both push‐pull and side‐to‐side movements of contralateral but not of ipsilateral arm. Relationship is different for push‐pull and side‐to‐side movements of contralateral arm.

Adapted from DeLong 60
Figure 4. Figure 4.

Activity of low‐frequency discharge bursting neuron in external pallidal segment, with monkey resting and during push‐pull movements of arm and leg. Discharge is consistently related to movements of the arm but not the leg.

Adapted from DeLong 60
Figure 5. Figure 5.

Activity of a high‐frequency discharge cell in external pallidal segment, with monkey resting and during push‐pull movements of arm and leg. Discharge is related to movements of the leg but not the arm.

Adapted from DeLong 60
Figure 6. Figure 6.

Activity of an internal globus pallidus neuron in raster form during 25 isometric pushing trials (above) and 25 pulling trials (below). Stimulus for each trial occurs at center bar. Interval to left of stimulus is a 500‐ms control period. For each trial the response (a threshold charge in AC‐coupled force) is indicated by thick vertical bar. Change in discharge during each trial occurred prior to onset of movement and was better locked to response than to stimulus. Activity of cell during steady pushing and pulling was also different.

From DeLong 61
Figure 7. Figure 7.

Distribution of earliest electromyographic changes (above) and earliest neural responses (below) in external globus pallidus (solid line) and internal globus pallidus (broken line) in relation to threshold force change in task used in force reversal task 61. Note that changes in discharge in some pallidal neurons clearly precede earliest electromyographic changes (100 ms), whereas majority of changes occur during period of electromyogram activation.

From data of DeLong 61
Figure 8. Figure 8.

Composite figure illustrating somatotopic grouping of movement‐related neurons in globus pallidus (GPe and GPi), subthalamic nucleus (STN), and pars reticulata substantia nigra (SNpr) of the monkey. Representative coronal sections from slightly different anteroposterior levels for each structure are shown. Location of neurons along individual penetrations are illustrated by the following symbols: leg, ▴; arm, •; and face, ○. A complete body representation is present in each segment of globus pallidus and subthalamic nucleus. Representation of each body part extends over almost entire anteroposterior extent of each structure (not shown). For pars reticulata of substantia nigra, note absence of arm‐ and leg‐related neurons and clustering of cells related to orofacial movements in lateral portions of nucleus as if a continuation of orofacial representation in GPi. Neurons in the pars compacta of the substantia nigra (SNpc,) exhibited little or no phasic changes in activity during movements of individual body parts.

From data of DeLong and Georgopoulos 65
Figure 9. Figure 9.

Activity of cell from putamen during pushing and pulling ballistic (A, B) and ramp (C, D) movements. For each case upper trace represents position of arm during a single trial; middle trace represents unit discharge for same trial; and lower portion represents activity of unit during 12 successive trials shown in raster form. Each trial is aligned on time of leaving zone (center bar). Interval from center bar to margin of raster is 1 s. This cell discharged prior to and during the first portion of both pushing and pulling ramp movements (C, D) but not during pushing or pulling ballistic movements (A, B). This cell, like most putamen neurons, was inactive during rest.

From DeLong 306. Copyright 1973 by the American Association for the Advancement of Science
Figure 10. Figure 10.

Activity of cell in monkey subthalamic nucleus during flexion arm movements of different amplitudes: S (small = 25 mm), M (medium = 62.5), and L (large = 100 mm). Trials for each class are aligned on response (R), first detectable change in velocity. A clear relationship of discharge to amplitude of movement can be seen. Activity of this cell was not modulated during extension.

From data of DeLong and Georgopoulos 65
Figure 11. Figure 11.

Relationship between maximum velocity achieved during a step and amplitude of the step in patients with parkinsonism (solid line) and 12 normal subjects (broken line). Data from 260 steps in five untreated parkinsonian patients and from 612 steps in 12 normal subjects were analyzed. Mean values of maximum velocity indicated by closed circles. Regression formula for patients was y = 0.51x + 0.59 and for normal subjects was y = 4.1x + 1.2. Shaded areas indicate ±1 SD of the estimated value of y.

From Draper and Johns 77. © 1964 by The Johns Hopkins University Press
Figure 12. Figure 12.

Schematic summary of main points of similarity in organization of cerebral connections of cerebellum and basal ganglia. Presumed equivalent pathways in two systems are shown by same kinds of symbols. Interrupted lines indicate possible connections. Ce, cerebellar cortex; D, dentate nucleus; F, fastigial nucleus; GPe, globus pallidus, external segment; GPi, globus pallidus, internal segment; I, interpositus nucleus; IL, intralaminar nuclei of thalamus; IO, inferior olive; M, motor cortex; N. Teg, tegmental nuclei; PN, pontine nuclei; RN, red nucleus; St, striatum; VL, ventrolateral nucleus of thalamus.

From Kemp and Powell 145
Figure 13. Figure 13.

Schematic diagram showing hypothetical integration of cortical inputs within putamen. Arm representation is chosen as an example. In putamen this representation consists of a long anteroposterior cylinder where inputs from “arm” representation in cortical areas 6, 4, 3, 2, 1, 5 are integrated. This cylindrical representation is maintained in pallidum and ventrolateral nucleus of thalamus by virtue of topographically organized connections. Main corticoputaminal projections are shown as heavy lines; projections from reciprocally interconnected cortical area are shown as continuous light lines and those from nonreciprocally connected areas as dashed lines.



Figure 1.

Schematic diagram of principal intrinsic and extrinsic connections of basal ganglia. GPe, external pallidal segment; GPi, internal pallidal segment; SNpr, substantia nigra pars reticulata; SNpc, substantia nigra pars compacta; STN, subthalamic nucleus; CM, center median; VL, n. ventralis lateralis; VA, n. ventralis anterior; SC, superior colliculus; RF, reticular formation; VTA, ventral tegmental area; TPC, n. tegmenti pedunculopontinus pars compacta. The dashed lines indicate dopamine pathways. Projections from the raphe to the striatum and substantia nigra have been omitted.



Figure 2.

Typical patterns of discharge observed during rest. GPe, external segment of globus pallidus; GPi, internal segment of globus pallidus; BORDER, “border” cells; S.I., substantia innominate cells. Cells in GPe fell into two groups: A: high‐frequency discharge neurons with recurrent long intervals and silence; and B: low‐frequency discharge bursting neurons. In contrast to GPe, cells in GPi (C) discharged in a continuous manner. Cells located along borders of the two pallidal segments (D) exhibited a fourth discharge pattern, similar to that of neurons in the substantia innominata (E).

From DeLong 60


Figure 3.

Activity of a high‐frequency discharge cell in external pallidal segment with monkey resting, during push‐pull (P‐P) and side‐to‐side (S‐S) movements of contralateral arm, and during push‐pull and side‐to‐side movements of ipsilateral arm. Line below unit represents position of rod. For push‐pull movements, up is for pull and down is for push; for side‐to‐side movements, up is for extension and down is for flexion. Discharge of this cell is phasically related to both push‐pull and side‐to‐side movements of contralateral but not of ipsilateral arm. Relationship is different for push‐pull and side‐to‐side movements of contralateral arm.

Adapted from DeLong 60


Figure 4.

Activity of low‐frequency discharge bursting neuron in external pallidal segment, with monkey resting and during push‐pull movements of arm and leg. Discharge is consistently related to movements of the arm but not the leg.

Adapted from DeLong 60


Figure 5.

Activity of a high‐frequency discharge cell in external pallidal segment, with monkey resting and during push‐pull movements of arm and leg. Discharge is related to movements of the leg but not the arm.

Adapted from DeLong 60


Figure 6.

Activity of an internal globus pallidus neuron in raster form during 25 isometric pushing trials (above) and 25 pulling trials (below). Stimulus for each trial occurs at center bar. Interval to left of stimulus is a 500‐ms control period. For each trial the response (a threshold charge in AC‐coupled force) is indicated by thick vertical bar. Change in discharge during each trial occurred prior to onset of movement and was better locked to response than to stimulus. Activity of cell during steady pushing and pulling was also different.

From DeLong 61


Figure 7.

Distribution of earliest electromyographic changes (above) and earliest neural responses (below) in external globus pallidus (solid line) and internal globus pallidus (broken line) in relation to threshold force change in task used in force reversal task 61. Note that changes in discharge in some pallidal neurons clearly precede earliest electromyographic changes (100 ms), whereas majority of changes occur during period of electromyogram activation.

From data of DeLong 61


Figure 8.

Composite figure illustrating somatotopic grouping of movement‐related neurons in globus pallidus (GPe and GPi), subthalamic nucleus (STN), and pars reticulata substantia nigra (SNpr) of the monkey. Representative coronal sections from slightly different anteroposterior levels for each structure are shown. Location of neurons along individual penetrations are illustrated by the following symbols: leg, ▴; arm, •; and face, ○. A complete body representation is present in each segment of globus pallidus and subthalamic nucleus. Representation of each body part extends over almost entire anteroposterior extent of each structure (not shown). For pars reticulata of substantia nigra, note absence of arm‐ and leg‐related neurons and clustering of cells related to orofacial movements in lateral portions of nucleus as if a continuation of orofacial representation in GPi. Neurons in the pars compacta of the substantia nigra (SNpc,) exhibited little or no phasic changes in activity during movements of individual body parts.

From data of DeLong and Georgopoulos 65


Figure 9.

Activity of cell from putamen during pushing and pulling ballistic (A, B) and ramp (C, D) movements. For each case upper trace represents position of arm during a single trial; middle trace represents unit discharge for same trial; and lower portion represents activity of unit during 12 successive trials shown in raster form. Each trial is aligned on time of leaving zone (center bar). Interval from center bar to margin of raster is 1 s. This cell discharged prior to and during the first portion of both pushing and pulling ramp movements (C, D) but not during pushing or pulling ballistic movements (A, B). This cell, like most putamen neurons, was inactive during rest.

From DeLong 306. Copyright 1973 by the American Association for the Advancement of Science


Figure 10.

Activity of cell in monkey subthalamic nucleus during flexion arm movements of different amplitudes: S (small = 25 mm), M (medium = 62.5), and L (large = 100 mm). Trials for each class are aligned on response (R), first detectable change in velocity. A clear relationship of discharge to amplitude of movement can be seen. Activity of this cell was not modulated during extension.

From data of DeLong and Georgopoulos 65


Figure 11.

Relationship between maximum velocity achieved during a step and amplitude of the step in patients with parkinsonism (solid line) and 12 normal subjects (broken line). Data from 260 steps in five untreated parkinsonian patients and from 612 steps in 12 normal subjects were analyzed. Mean values of maximum velocity indicated by closed circles. Regression formula for patients was y = 0.51x + 0.59 and for normal subjects was y = 4.1x + 1.2. Shaded areas indicate ±1 SD of the estimated value of y.

From Draper and Johns 77. © 1964 by The Johns Hopkins University Press


Figure 12.

Schematic summary of main points of similarity in organization of cerebral connections of cerebellum and basal ganglia. Presumed equivalent pathways in two systems are shown by same kinds of symbols. Interrupted lines indicate possible connections. Ce, cerebellar cortex; D, dentate nucleus; F, fastigial nucleus; GPe, globus pallidus, external segment; GPi, globus pallidus, internal segment; I, interpositus nucleus; IL, intralaminar nuclei of thalamus; IO, inferior olive; M, motor cortex; N. Teg, tegmental nuclei; PN, pontine nuclei; RN, red nucleus; St, striatum; VL, ventrolateral nucleus of thalamus.

From Kemp and Powell 145


Figure 13.

Schematic diagram showing hypothetical integration of cortical inputs within putamen. Arm representation is chosen as an example. In putamen this representation consists of a long anteroposterior cylinder where inputs from “arm” representation in cortical areas 6, 4, 3, 2, 1, 5 are integrated. This cylindrical representation is maintained in pallidum and ventrolateral nucleus of thalamus by virtue of topographically organized connections. Main corticoputaminal projections are shown as heavy lines; projections from reciprocally interconnected cortical area are shown as continuous light lines and those from nonreciprocally connected areas as dashed lines.

References
 1. Akert, K., and B. Andersson. Experimenteller Beitrag zur Pysiologie des Nucleus Caudatus. Acta Physiol. Scand. 22: 281–298, 1951.
 2. Albe‐Fessard, D., G. Guiot, Y. Lammare, and G. Arfel. Activation of thalamocortical projections related to tremorogenic processes. In: The Thalamus, edited by D. P. Purpura and M. D. Yahr. New York: Columbia Univ. Press, 1966, p. 237–253.
 3. Albe‐Fessard, D., C. Rocha‐Miranda, and E. Oswaldo‐Cruz. Activités évoquées dans le noyau caudé du chat en résponse à des types divers d'afférents. II. Étude microphysiologique. Electroencephalogr. Clin. Neurophysiol. 12: 649–661, 1960.
 4. Aldridge, J. W., R. J. Anderson, and J. T. Murphy. Responses of caudate neurons in awake monkeys to a visual stimulus that initiates a motor task. Soc. Neurosci. Abstr. 4: 41, 1978.
 5. Allen, G. I., and N. Tsukahara. Cerebrocerebellar communication systems. Physiol. Rev. 54: 957–1006, 1974.
 6. Amato, G., E. Trouche, D. Beaubaton, and A. Grangetto. The role of internal pallidal segment on the initiation of a goaldirected movement. Neurosci. Lett. 9: 159–163, 1978.
 7. Andén, N. E., and B. Johnels. Effect of local application of apomorphine to the corpus striatum and to the nucleus accumbens on the reserpine‐induced rigidity in rats. Brain Res. 133: 386–389, 1977.
 8. Anderson, M. E. Tonic firing of substantia nigra neurons in awake monkeys. Soc. Neurosci. Abstr. 2: 59, 1976.
 9. Anderson, M. E. Discharge patterns of basal ganglia neurons during active maintenance of postural stability and adjustment to chair tilt. Brain Res. 143: 325–338, 1977.
 10. Anderson, R. J., J. W. Aldridge, and J. T. Murphy. Somatic and visual feedback to monkey caudate nucleus during a central motor program. Soc. Neurosci. Abstr. 2: 59, 1976.
 11. Angel, R. W., W. Alston, and H. Garland. l‐Dopa and error correction time in Parkinson's disease. Neurology 21: 1255–1260, 1971.
 12. Angel, R. W., W. Alston, and J. R. Higgins. Control of movement in Parkinson's disease. Brain 93: 1–14, 1970.
 13. Arvidsson, J., I. Jurna, and G. Steg. Striatal and spinal lesions eliminating reserpine and physostigmine rigidity. Life Sci. 6: 2017–2020, 1967.
 14. Battista, A. F., M. Goldstein, and M. Ogawa. Production of involuntary movements by l‐dopa in monkeys with tegmental lesions. Exp. Neurol. 33: 566–575, 1971.
 15. von Bechterew, U. Die Functionen der Nervencentra. Jena: Fischer, 1909, vol. 2. p. 1232–1255.
 16. Beck, E., and A. Bignami. Some neuro‐anatomical observations in cases with stereotactic lesions for the relief of Parkinsonism. Brain 91: 589–618, 1968.
 17. bédard, P., I. larochelle, L. J. poirier, and T. L. Sourkes. Reversible effects of l‐dopa on tremor and catatonia induced by alpha‐methyl‐p‐tyrosine. Can. J. Physiol. Pharmacol. 48: 82–84, 1970.
 18. Bergouignan, M., and P. Verger. Les réactions labyrinthiques chez le chien après lésions d'un noyau caudé. C. R. Soc. Biol. Paris 118: 1539–1541, 1935.
 19. Brodal, P. The corticopontine projection in the rhesus monkey: origin and principles of organization. Brain 101: 251–283, 1978.
 20. Brozoski, T. J., R. M. Brown, H. E. Rosvold, and P. S. Goldman. Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Science 205: 929–931, 1979.
 21. Buchwald, N. A., and F. R. Ervin. Evoked potentials and behavior. A study of responses to subcortical stimulation in the awake, unrestrained animal. Electroencephalogr. Clin. Neurophysiol. 9: 477–496, 1957.
 22. Buchwald, N. A., C. D. Hull, M. D. Levine, and J. R. Villablanca. The basal ganglia and the regulation of response and cognitive sets. In: Growth and Development of the Brain: Nutritional, Genetic, and Environmental Factors, edited by M. A. B. Brazier. New York: Raven, 1975, p. 171–189.
 23. Buchwald, N. A., C. D. Hull, and M. C. Trachtenberg. Concomitant behavioral and neural inhibition and disinhibition in response to subcortical stimulation. Exp. Brain Res. 4: 58–72, 1967.
 24. Bucy, P. C. Is there a pyramidal tract? Brain 80: 376–392, 1957.
 25. Bucy, P. C., and D. N. Buchanan. Athetosis. Brain 55: 479–492, 1932.
 26. Burke, D., E. Hagbarth, and B. G. Wallin. Reflex mechanisms in Parkinsonian rigidity. Scand. J. Rehabil. Med. 9: 15–23, 1977.
 27. Buser, P., G. Poudereux, and J. Mereaux. Single unit recording in the caudate nucleus during sessions with elaborate movement in the awake monkey. Brain Res. 71: 337–344, 1974.
 28. Campbell, K. M., and R. E. Dill. Trunk rigidity and limb hypotonia produced in squirrel monkeys by direct cholinergic stimulation of the globus pallidus. Exp. Neurol. 42: 555–565, 1974.
 29. Cannon, B. W., H. W. Magoun, and W. F. Windle. Paralysis without hypotonicity and hyperreflexia subsequent to section of basis pedunculi in monkeys. J. Neurophysiol. 7: 425–437, 1944.
 30. Carey, J. H. Certain anatomical and functional interrelations between the tegmentum of the midbrain and the basal ganglia. J. Comp. Neurol. 108: 57–89, 1957.
 31. Carey, J. H., and R. N. DeJong. Preliminary studies on the production of Parkinson's syndrome. Trans. Am. Neurol. Assoc. 79: 28–35, 1954.
 32. Carpenter, M. B., and C. S. Carpenter. Analysis of somatotopic relations of corpus luysi in man and monkey: relation between site of dyskinesia and distribution of lesions within subthalamic nucleus. J. Comp. Neurol. 95: 349–370, 1951.
 33. Carpenter, M. B., and R. E. McMasters. Lesions of the substantia nigra in the rhesus monkey. Efferent fiber degeneration and behavioral observations. Am. J. Anat. 114: 293–320, 1964.
 34. Carpenter, M. B., and F. A. Mettler. Analysis of subthalamic hyperkinesia in the monkey, with special reference to ablations of agranular cortex. J. Comp. Neurol. 95: 125–158, 1951.
 35. Carpenter, M. B., and P. Peter. Nigrostriatal and nigrothalamic fibers in the rhesus monkey. J. Comp. Neurol. 144: 94–166, 1972.
 36. Carpenter, M. B., and N. L. Strominger. Efferent fibers of the subthalamic nucleus in monkey. A comparison of the efferent projections of the subthalamic nucleus, substantia nigra and globus pallidus. Am. J. Anat. 121: 47–72, 1967.
 37. Carpenter, M. B., and J. R. Whittier. Study of methods for producing experimental lesions of the central nervous system with special reference to the stereotaxic technique. J. Comp. Neurol. 97: 73–132, 1952.
 38. Carpenter, M. B., J. W. Correll, and A. Hinman. Spinal tracts mediating subthalamic hyperkinesia. Physiological effects of selective partial cordotomies upon dyskinesia in rhesus monkey. J. Neurophysiol. 23: 288–304, 1960.
 39. Carpenter, M. B., R. A. R. Fraser, and J. E. Shriver. The organization of pallidosubthalamic fibers in the monkey. Brain Res. 11: 522–559, 1968.
 40. Carpenter, M. B., K. Nakano, and R. Kim. Nigrothalamic projections in the monkey demonstrated by autoradiographic techniques. J. Comp. Neurol. 165: 401–416, 1976.
 41. Carpenter, M. B., N. L. Stominger, and A. H. Weiss. Effects of lesions in the intralaminar thalamic nuclei upon subthalamic dyskinesia: a study in the rhesus monkey Arch. Neurol. Chicago 13: 113–125, 1965.
 42. Carpenter, M. B., J. R. Whittier, and F. A. Mettler. Analysis of choreoid hyperkinesia in the rhesus monkey. Surgical and pharmacological analysis of hyperkinesia resulting from lesions of the subthalamic nucleus of Luys. J. Comp. Neurol. 92: 293–331, 1950.
 43. Carrea, R. M. E., and F. A. Mettler. Function of the brachium conjunctivum and related structures. J. Comp. Neurol. 102: 151–322, 1955.
 44. Cassell, K., K. Shaw, and G. Stern. A computerised tracking technique for the assessment of Parkinsonian motor disability. Brain 96: 815–826, 1973.
 45. Caveness, W. F., M. Kato, B. L. Malamut, S. Hosokawa, S. Wakisaka, and R. R. O'Neill. The propagation of focal motor seizures in the monkey. Ann. Neurol. 7: 213–221, 1980.
 46. Chandler, W. F., and E. C. Crosby. Motor effects of stimulation and ablation of the caudate nucleus of the monkey. Neurology 25: 1160–1163, 1975.
 47. Cooke, J. D., J. D. Brown, V. B. Brooks. Increased dependence on visual information for movement control in patients with Parkinson's disease. Can. J. Neurol. Sci. 5: 413–415, 1978.
 48. Cools, A. R. Athetoid and choreiform hyperkinesias produced by caudate application of dopamine in cats. Psychopharmacologia 25: 229–237, 1972.
 49. Cools, A. R. Chemical and electrical stimulation of the caudate nucleus in freely moving cats: the role of dopamine. Brain Res. 58: 437–451, 1973.
 50. Cooper, I. S. Surgical occlusion of the anterior choroidal artery in Parkinsonism. Surg. Gynecol. Obstet. 99: 207–219, 1954.
 51. Cooper, I. S. Twenty year follow‐up study of the neurosurgical treatment of dystonia musculorum deformans. Adv. Neurol. 14: 423–452, 1976.
 52. Cooper, I. S., and N. Poloukhine. The globus pallidus as a surgical target. J. Am. Geriatr. Soc. 4: 1182–1207, 1956.
 53. Cordeau, J. P., and Y. Lamarre. Further studies on patterns of central unit activity in relation with tremor. J. Neurosurg. 24: 213–218, 1966.
 54. Cordeau, J. P., J. Gybels, H. H. Jasper, and L. J. Poirier. Microelectrode studies of unit discharges in the sensorimotor cortex: investigation in monkeys with experimental tremor. Neurology 10: 591–600, 1960.
 55. Cowan, W. M., and T. P. S. Powell. Strio‐pallidal projection in the monkey. J. Neurol. Neurosurg. Psychiatry 29: 426–439, 1966.
 56. Crossman, A. R., and M. A. Sambrook. Experimental torticollis in the monkey produced by unilateral 6‐hydroxydopamine brain lesions. Brain Res. 149: 498–502, 1978.
 57. Davison, C., and S. P. Goodheart. Monochorea and somatotopic localization. Arch. Neurol. Psychiatry 43: 792–803, 1940.
 58. DeAjuriaguerra, J. The concept of akinesia. Psychol. Med. 5: 129–131, 1975.
 59. Delgado, J. M. R., J. M. Delgado‐Garcia, J. A. Americo, and C. Grau. Behavioral inhibition induced by pallidal stimulation in monkeys. Exp. Neurol. 49: 580–591, 1975.
 60. Delgado, J. M. R., J. M. Delgado‐Garcia, M. Conde, and S. S. Robles. Fatigability of caudate nucleus stimulation in cats. Neuropsychologia 14: 11–21, 1976.
 61. DeLong, M. R. Activity of pallidal neurons during movement. J. Neurophysiol. 34: 414–427, 1971.
 62. DeLong, M. R. Activity of basal ganglia neurons during movement. Brain Res. 40: 127–135, 1972.
 63. DeLong, M. R., Motor functions of the basal ganglia: single‐unit activity during movement. In: Neurosciences, Third Study Program, edited by F. O. Schmitt and F. G. Worden. Cambridge: MIT Press, 1974, p. 319–324.
 64. DeLong, M. R. Putamen: activity of single units during slow and rapid arm movements. Science 179: 1240–1242, 1973.
 65. DeLong, M. R., and J. T. Coyle. Globus passidus lesions in the monkey produced by kainic acid: histologic and behavioral effects. Appl. Neurophysiol. 42: 95–97, 1979.
 66. DeLong, M. R., and A. P. Georgopoulos. The subthalamic nucleus and the substantia nigra of the monkey. Neuronal activity in relation to movement. Soc. Neurosci. Abstr. 4: 42, 1978.
 67. DeLong, M. R., and A. P. Georgopoulos. Motor function of the basal ganglia as revealed by studies of single cell activity in the behaving primate. Adv. Neurol. 24: 131–140, 1979.
 68. DeLong, M. R., and A. P. Georgopoulos. Physiology of the basal ganglia. A brief overview. Adv. Neurol. 24: 137–152, 1979.
 69. DeLong, M. R., and P. L. Strick. Relation of basal ganglia, cerebellum, and motor cortex units to ramp and ballistic limb movements. Brain Res. 71: 327–335, 1974.
 70. Denny‐Brown, D. The Basal Ganglia and Their Relation to Disorders of Movement. London: Oxford Univ. Press, 1962.
 71. Denny‐Brown, D., and N. Yanagisawa. The role of the basal ganglia in the initiation of movement. In: The Basal Ganglia, edited by M. D. Yahr. New York: Raven, 1976, p. 115–148.
 72. Dieckmann, G., and R. Hassler. Reizexperimente zur Function des Putamen der Katze. J. Hirnforsch. 10: 187–225, 1968.
 73. Dieckmann, G., and K. Sasaki. Recruiting responses in the cerebral cortex produced by putamen and pallidum stimulation. Exp. Brain Res. 10: 236–250, 1970.
 74. Dietrichson, P. Phasic ankle reflex in spasticity and Parkinson rigidity. The role of the fusimotor system. Acta Neurol. Scand. 47: 22–51, 1971.
 75. Dietrichson, P. Tonic ankle reflex in Parkinsonian rigidity and in spasticity. The role of the fusimotor system. Acta Neurol. Scand. 47: 163–182, 1971.
 76. Divac, I. Drug‐induced syndromes in rats with large, chronic‐lesions in the corpus striatum. Psychopharmacologia 21: 171–178, 1972.
 77. Divac, I., Does the neostriatum operate as a functional entity? In: Psychobiology of the Striatum, edited by A. R. Cools, A. H. M. Lohman, and J. H. L. Van den Bercken. Amsterdam: Elsevier, 1977, p. 21–30.
 78. Dolbakyan, E., N. Hernandez‐Mesa, and J. Bureš. Skilled forelimb movements and unit activity in motor cortex and caudate nucleus in rats. Neuroscience 2: 73–80, 1977.
 79. Draper, I. T., and R. J. Johns. The disordered movement in parkinsonism and the effect of drug treatment. Bull. Johns Hopkins Hosp. 115: 465–480, 1964.
 80. Ellinwood, E. H. Effect of chronic methamphetamine intoxication in rhesus monkeys. Biol. Psychiatry 3: 25–32, 1971.
 81. Ernst, A. M., and P. G. Smelik. Site of action of dopamine and apomorphine on compulsive gnawing behavior in rats. Experientia 22: 837–838, 1966.
 82. Essig, C. F., J. L. Hampson, A. McCauley, and H. E. Himwich. An experimental analysis of biochemically induced circling behavior. J. Neurophysiol. 13: 269–275, 1950.
 83. Evarts, E. V. Pyramidal tract activity associated with a conditioned hand movement in the monkey. J. Neurophysiol. 29: 1011–1027, 1966.
 84. Evarts, E. V., and W. T. Thach. Motor mechanism of the CNS: cerebrocerebellar interrelations. Annu. Rev. Physiol. 31: 451–498, 1969.
 85. Evarts, E. V., H. T. Teräväinen, D. E. Beuchert, and D. B. Calne. Pathophysiology of motor performance in Parkinson's disease. In: Dopaminergic Ergot Derivatives and Motor Functions, edited by K. Fuchs and D. B. Calne. New York: Pergamon, 1979, p. 45–69.
 86. Fallon, J. H., and R. Y. Moore. Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J. Comp. Neurol. 180: 545–580, 1978.
 87. Filion, M. Effects of interruption of the nigrostriatal pathway and of dopaminergic agents on the spontaneous activity of globus pallidus neurons in the awake monkey. Brain Res. 178: 425–441, 1979.
 88. Flowers, K. A. Visual ‘closed loop' and ‘open loop' characteristics of voluntary movement in patients with parkinsonism and intention tremor. Brain 99: 269–310, 1976.
 89. Flowers, K. A. Some frequency response characteristics of Parkinsonism on pursuit tracking. Brain 101: 19–34, 1978.
 90. Fog, R., A. Randrup, and H. Pakkenberg. Lesions in the corpus striatum and cortex of rat brains and the effect on pharmacologically induced stereotyped agressive and cataleptic behavior. Psychopharmacologia 18: 346–356. 1970.
 91. Foix, C. E., and J. Nicolesco. Anatomie cérébrate. Les noyaux gris centraux et la région mésencéphalo‐sousoptique. Paris: Masson, 1925.
 92. Forman, D., and J. W. Ward. Responses to electrical stimulation of caudate nucleus in cats in chronic experiments. J. Neurophysiol. 20: 230–244, 1957.
 93. Freeman, G. L., and L. Krasno. Inhibitory functions of the corpus striatum. Arch. Neurol. Psychiatry 44: 323–327, 1940.
 94. Georgopoulos, A. P., and M. R. DeLong. The globus pallidus of the monkey: neuronal activity in relation to movement. Soc. Neurosci. Abstr. 4: 43, 1978.
 95. Georgopoulos, A. P., and M. R. DeLong. Quantitative studies of movement‐related neurons in the basal ganglia of behaving monkeys. Can. J. Neurol. Sci. 6: 79, 1979.
 96. Gerebtzoff, M. A. Contribution à la physiologie du corps strié. Arch. Int. Physiol. Biochim. 51: 333–353, 1941.
 97. Goldman, P. S., and W. J. Nauta. An intricately patterned pre‐fronto‐caudate projection in the rhesus monkey. J. Comp. Neurol. 171: 369–386, 1977.
 98. Goldman, P. S., and H. E. Rosvold. The effects of selective caudate lesions in infant and juvenile rhesus monkeys. Brain Res. 43: 53–66, 1972.
 99. Goldstein, M., B. Anagnoste, W. S. Owen, and A. F. Battista. The effects of ventromedial tegmental lesions in the biosynthesis of catecholamines in the striatum. Life Sci. 5: 2171, 1966.
 100. Gorry, J. D. Studies on the comparative anatomy of the ganglion of Meynert. Acta Anat. 55: 51–104, 1963.
 101. Graybiel, A. M. Organization of the nigrotectal connection: an experimental tracer study in the cat. Brain Res. 143: 339–348, 1978.
 102. Greenfield, J. G., and F. D. Bosanquet. The brain‐stem lesions in parkinsonism. J. Neurol. Neurosurg. Psychiatry 16: 213–226, 1953.
 103. Grofová, I. The identification of striatal and pallidal neurons projecting to substantia nigra. An experimental study by means of retrograde axonal transport of horseradish peroxidase. Brain Res. 91: 286–291, 1975.
 104. Gybels, J., M. Meulders, M. Callens, and J. Colle. Disturbances of visuo‐motor integration in cats with small lesions of the caudate nucleus. Arch. Int. Physiol. Biochim. 75: 283–302, 1967.
 105. Hallet, M., B. T. Shanani, and R. R. Young. Analysis of stereotyped voluntary movements at the elbow in patients with Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 40: 1129–1135, 1977.
 106. Hardy, J., and C. Bertrand. Electrophysiological localization and identification. J. Neurosurg. 24: 410–414, 1966.
 107. Harik, S. I., and P. L. Morris. The effects of lesions in the head of the caudate nucleus on spontaneous and l‐dopa induced activity in the cat. Brain Res. 62: 279–285, 1973.
 108. Harper, J. A., and T. I. Lidsky. Trigeminal influences on caudate and substantia nigra units. Soc. Neurosci. Abstr. 3: 38, 1977.
 109. Hartmann‐Von Monakow, K., K. Akert, and H. Künzle. Projections of the precentral motor cortex and other cortical areas of the frontal lobe to the subthalamic nucleus in the monkey. Exp. Brain Res. 33: 395–403, 1978.
 110. Harvey, R. J., R. Porter, and J. A. Rawson. The natural discharges of Purkinje cells in paravermal regions of lobules V and VI of the monkey's cerebellum. J. Physiol. London 271: 515–536, 1977.
 111. Hassler, R. Die zentralen Apparate der Wendebewegungen, Parts I and II. Arch. Psychiatr. Nervenkr. 194: 456–480, 481–516, 1956.
 112. Hassler, R. Striatal control of locomotion, intentional actions and of integrating and perceptive activity. J. Neurol. Sci. 36: 187–224, 1978.
 113. Hassler, R., and G. Dieckmann. Arrest reaction, delayed inhibition and unusual gaze behavior resulting from stimulation of the putamen in awake, unrestrained cats. Brain Res. 5: 504–508, 1967.
 114. Hassler, R., and G. Dieckmann. Locomotor movements in opposite directions induced by stimulation of pallidum or of putamen. J. Neurol. Sci. 8: 189–195, 1968.
 115. Hassler, R., and T. Reichert. Indikationen und Lokalisationsmethode der gezielten Hirnoperationen. Nervenarzt 25: 441–447, 1954.
 116. Hassler, R., F. Mundinger, and T. Reichert. Correlations between clinical and autoptic findings in stereotaxic operations of parkinsonism. Confin. Neurol. 26: 282–290, 1965.
 117. Hassler, R., T. Reichert, F. Mundinger, W. Umbach, and J. A. Ganglberger. Physiological observations in stereotaxic operations in extrapyramidal motor disturbances. Brain 83: 337–350, 1960.
 118. Heath, R. G., and R. Hodes. Induction of sleep by stimulation of the caudate nucleus in macaque rhesus and man. Trans. Am. Neurol. Assoc. 77: 204–210, 1952.
 119. Heilman, K. M., D. Bowers, R. T. Watson, and M. Greer. Reaction times in Parkinson's disease. Arch. Neurol. Chicago 33: 139–140, 1976.
 120. Heimer, L., The olfactory cortex and the ventral striatum. In: Limbic Mechanisms: The Continuing Evaluation of the Limbic System Concept, edited by K. E. Livingston and O. Hornykiewicz. New York: Plenum, 1978, p. 95–197.
 121. Herkenham, M. Intralaminar and parafascicular efferents to the striatum and cortex in the rat: an autoradiographic study. Anat. Rec. 190: 429, 1978.
 122. Hodes, R., S. M. Peacock, Jr., and R. G. Heath. Influences of the forebrain on somato‐motor activity. I. Inhibition. J. Comp. Neurol. 94: 381–408, 1951.
 123. Hopkins, D., and L. W. Niessen. Substantia nigra projections to the reticular formation, superior colliculus, and central gray in the rat, cat, and monkey. Neurosci. Lett. 2: 253–259, 1976.
 124. Hore, J., J. Meyer‐Lohmann, and V. B. Brooks. Basal ganglia cooling disables learned arm movements of monkeys in the absence of visual guidance. Science 195: 585–586, 1977.
 125. Hore, J., and T. Vilis. Arm movement performance during reversible basal ganglia lesions in the monkey. Exp. Brain Res. 39: 217–228, 1980.
 126. Horne, D. J. Sensorimotor control in parkinsonism. J. Neurol. Neurosurg. Psychiatry 36: 742–746, 1973.
 127. Hornykiewicz, O. Dopamine (3‐hydroxytyramine) and brain function. Pharmacol. Rev. 18: 925–964, 1966.
 128. Horsley, V. The function of the so‐called motor area of the brain. Br. Med. J. 2: 125–132, 1909.
 129. Hull, C. D., N. A. Buchwald, and G. Ling. Effects of direct cholinergic stimulation of forebrain structures. Brain Res. 6: 22–35, 1967.
 130. Iversen, S. D., Brain dopamine systems and behavior. In: Handbook of Psychopharmacology, edited by L. L. Iversen, S. D. Iversen, and S. H. Snyder. New York: Plenum, vol. 8, 1977, p. 333–384.
 131. Iversen, S. D., Striatal function and stereotyped behavior. In: Psychobiology of the Striatum, edited by A. R. Cools, A. H. M. Lohman, and J. H. L. Van den Bercken. Amsterdam: Elsevier, 1977, p. 99–118.
 132. Jackson, D. M., N. E. Andén, and A. Dahlström. A functional effect of dopamine in the nucleus accumbens and in some other dopamine‐rich parts of the rat brain. Psychopharmacologia 45: 139–149, 1975.
 133. Jacobson, S., N. Butters, and N. J. Tovsky. Afferent and efferent subcortical projections of behaviorally defined sectors of prefrontal granular cortex. Brain Res. 159: 279–296, 1978.
 134. Jasper, H. H., and G. Bertrand. Recording from microelectrodes in stereotaxic surgery for Parkinson's disease. J. Neurosurg. 23: 219–221, 1966.
 135. Jayaraman, A., R. Batton, and M. B. Carpenter. Nigrotectal projections in the monkey: an autoradiographic study. Brain Res. 135: 147–152, 1977.
 136. Jellinger, K., Degenerations and exogenous lesions of the pallidum and striatum. In: Handbook of Clinical Neurology: Diseases of the Basal Ganglia, edited by P. J. Vinken and G. W. Bruyn. Amsterdam: North‐Holland, vol. 6, 1968, p. 631–693.
 137. Joffroy, A. J., and Y. Lamarre. Rhythmic unit firing in the precentral cortex in relation with postural tremor in a deafferented limb. Brain Res. 27: 386–389, 1971.
 138. Johnels, G., G. Steg, and U. Ungerstedt. A method for mechanographical recording of muscle tone in the rat. The affect of some antiparkinsonian drugs on rigidity induced by reserpine. Brain Res. 140: 177–181, 1978.
 139. Johnson, T. N., and H. E. Rosvold. Topographic projections on the globus pallidus and the substantia nigra of selectively placed lesions in the precommissural caudate nucleus and putamen in the monkey. Exp. Neurol. 33: 584–596, 1971.
 140. Jones, E. G., and R. Y. Leavitt. Retrograde axonal transport and the demonstration of non‐specific projections to the cerebral cortex and striatum from thalamic intralaminar nuclei in the rat, cat, and monkey. J. Comp. Neurol. 154: 349–378, 1974.
 141. Jones, E. G., J. D. Coulter, H. Burton, and R. Porter. Cells of origin and terminal distribution of corticostriatal fibers arising in the sensory‐motor cortex of monkeys. J. Comp. Neurol. 173: 53–80, 1977.
 142. Jung, R., and R. Hassler. The extrapyramidal motor system. In: Handbook of Physiology: Neurophysiology, edited by J. Field, H. W. Magoun, and V. E. Hall. Washington, DC: Am. Physiol. Soc., 1960, sect. 1, vol. II, chapt. 35, p. 863–927.
 143. Jungberg, T. I., and U. Ungerstedt. Sensory inattention produced by 6‐hydroxydopamine‐induced degeneration of ascending dopamine neurons. Exp. Neurol. 53: 585–600, 1976.
 144. Kalil, K. Patch‐like termination of thalamic fibers in the putamen of the rhesus monkey: an autoradiographic study. Brain Res. 140: 333–339, 1978.
 145. Kelly, P. H., Drug‐induced motor behavior. In: Handbook of Psychopharmacology, edited by L. L. Iversen, S. D. Iversen, and S. H. Snyder. New York: Plenum, 1978. vol. 8, p. 295–331.
 146. Kemp, J. M., and T. P. S. Powell. The cortico‐striate projection in the monkey. Brain 93: 525–546, 1970.
 147. Kemp, J. M., and T. P. S. Powell. The connexions of the striatum and globus pallidus: synthesis and speculation. Phil. Trans. Roy. Soc. London Ser. B. 262: 441–457, 1971.
 148. Kennard, M. A. Experimental analysis of the functions of the basal ganglia in monkeys and chimpanzees. J. Neurophysiol. 7: 127–148, 1944.
 149. Kievit, J., and H. G. J. M. Kuypers. Organization of the thalamo‐cortical connections to the frontal lobe in the rhesus monkey. Exp. Brain Res. 29: 299–322, 1977.
 150. Kim, R., K. Nakano, A. Jayaraman, and M. B. Carpenter. Projections of the globus pallidus and adjacent structures: an autoradiographic study in the monkey. J. Comp. Neurol. 169: 263–290, 1976.
 151. Kitai, S. T., R. J. Preston, G. A. Bishop, and J. D. Kocsis. Striatal projection neurons: morphological and electrophysiological studies. Adv. Neurol. 24: 45–51, 1979.
 152. Kitsikis, A. The suppression of arm movements in monkeys: threshold variations of caudate nucleus stimulation. Brain Res. 10: 460–462, 1968.
 153. Kitsikis, A., and A. Rougel. The effect of caudate stimulation on conditioned motor behavior in monkeys. Physiol. Behav. 3: 831–837, 1968.
 154. Kitsikis, A., L. Angyan, and P. Buser. Basal ganglia unitary activity during motor performance in monkeys. Physiol. Behav. 6: 609–611, 1971.
 155. Kitsikis, A., F. E. Horvath, and A. Rougeul. Synchronized spindle activity in the cortex of the monkey by basal ganglia stimulation. Electroencephalogr. Clin. Neurophysiol. 25: 160–169, 1968.
 156. Klawans, H. L., H. Moses, P. A. Nausieda, D. Berger, and W. J. Weiner. Treatment and prognosis of hemiballismus. N. Engl. J. Med. 295: 1348–1350, 1976.
 157. Knott, J. R., W. R. Ingram, and R. E. Correll. Some effects of subcortical stimulation on the bar press response. Arch. Neurol. Chicago 2: 130–138, 1960.
 158. Kornhuber, H. H. Motor functions of cerebellum and basal ganglia: the cerebellocortical saccadic (ballistic) clock, the cerebellonuclear hold regulator, and the basal ganglia ramp (voluntary speed smooth movement) generator. Kybernetik 8: 157–162, 1971.
 159. Krauthamer, G. M., Sensory functions of the neostriatum. In: The Neostriatum, edited by I. Divac and R. G. E. Oberg. Oxford: Pergamon, 1979, p. 263–290.
 160. Künzle, H. Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia: an autoradiographic study in Macaca fascicularis. Brain Res. 88: 195–209, 1975.
 161. Künzle, H. Thalamic projections from the precentral motor cortex in Macaca fascicularis. Brain Res. 105: 253–267, 1976.
 162. Künzle, H. An autoradiographic analysis of the efferent connections from premotor and adjacent prefrontal regions (areas 6 and 9) in Macaca fascicularis. Brain Behav. Evol. 15: 185–234, 1978.
 163. Kuo, J. S., and M. B. Carpenter. Organization of pallidothalamic projections in the rhesus monkey. J. Comp. Neurol. 151: 201–236, 1973.
 164. Lamarre, Y., and A. J. Joffroy. Thalamic unit activity in monkey with experimental tremor. In: L‐Dopa and Parkinsonism, edited by A. Barbeau and F. H. McDowell. Philadelphia: Davis, 1970, p. 163–170.
 165. Larochelle, L., P. Bédard, L. J. Poirier, and T. L. Sourkes. Correlative neuroanatomical and neuropharmacological study of tremor and catatonia in the monkey. Neuropharmacology 10: 273–288, 1971.
 166. Laursen, A. M. An experimental study of the pathways from the basal ganglia. J. Comp. Neurol. 102: 1–25, 1955.
 167. Laursen, A. M. Inhibition evoked from the region of the caudate nucleus in cats. Acta Physiol. Scand. 54: 185–190, 1962.
 168. Laursen, A. M. Movements evoked from the region of the caudate nucleus in cats. Acta Physiol. Scand. 54: 175–184, 1962.
 169. Laursen, A. M. The “extrapyramidal system” Acta Physiol. Scand (Suppl. 211) 59: 11–106, 1963.
 170. Liddell, E. G. T., and C. G. Phillips. Experimental lesions in the basal ganglia of the cat. Brain 63: 264–274, 1940.
 171. Lidsky, T. I., N. A. Buchwald, C. D. Hull, and M. S. Levine. Pallidal and entopeduncular single unit activity in cats during drinking. Electroencephalogr. Clin. Neurophysiol. 39: 79–84, 1975.
 172. Lidsky, T. I., J. H. Robinson, F. J. Denaro, and P. M. Winhold. Trigeminal influences on entopeduncular units. Brain Res. 141: 227–234, 1978.
 173. Liles, S. L. Functional organization of neurons related to arm movement in the putamen. Soc. Neurosci. Abstr. 4: 46, 1978.
 174. Liles, S. L. Unit activity in the putamen associated with conditioned arm movements: topographic organization. Federation Proc. 27: 396, 1978.
 175. Liles, S. L., and G. D. Davis. Athetoid and choreiform hyperkinesias produced by caudate lesions in the cat. Science 164: 195–197, 1969.
 176. Liles, S. L., and G. D. Davis. Interrelation of caudate nucleus and thalamus in alteration of cortically induced movement. J. Neurophysiol. 32: 564–573, 1969.
 177. Ljungberg, T., and U. Ungerstedt. Coagulation lesions of hypothalamus—no response with levo‐dopa. Physiol. Behav. 16: 277–283, 1976.
 178. MacLean, P. D. Effects of lesions of globus pallidus on species typical display behavior of squirrel monkeys. Brain Res. 149: 175–196, 1978.
 179. Magendie, F. Leçons sur les fonctions et les maladies du système nerveux. Paris: James, 1841.
 180. Marshall, J. R., and U. Ungerstedt. Striatal efferent fibers play a role in maintaining rotational behavior in the rat. Science 198: 62–64, 1977.
 181. Martin, J. P. The Basal Ganglia and Posture. Philadelphia: Lippincott, 1967.
 182. Martin, J. P., and I. R. McCaul. Acute hemiballismus treated by ventrolateral thalamolysis. Brain 82: 104–108, 1959.
 183. Mason, S. T., P. R. Sanberg, and H. C. Fibiger. Kainic acid lesions of the striatum dissociate amphetamine and apomorphine stereotypy: similarities to Huntington's chorea. Science 201: 352–355, 1978.
 184. Matsunami, K., and B. Cohen. Afferent modulation of unit activity in globus pallidus and caudate nucleus: changes induced by vestibular nucleus and pyramidal tract stimulation. Brain Res. 91: 140–146, 1975.
 185. McGuinness, C. M., E. Dalsass, E. Proshansky, and G. M. Krauthamer. Afferent connections of the nucleus centrum medianum in the cat. Soc. Neurosci. Abstr. 2: 67, 1976.
 186. McKenzie, G. M. Role of the tuberculum olfactorium on stereotyped behavior induced by apomorphine in the rat. Psychopharmacologia 23: 212–219, 1972.
 187. McLennan, H., P. R. Emmons, and P. M. Plummer. Some behavioral effects of stimulation of the caudate nucleus in unrestrained cats. Can. J. Physiol. Pharmacol. 42: 329–339, 1964.
 188. Mehler, W. R., Further notes on the centre median nucleus of Luys. In: The Thalamus, edited by D. P. Purpura and M. D. Yahr. New York: Columbia Univ. Press, 1966, p. 109–127.
 189. Melville Jones, G. M., and J. D. DeJong. Dynamic characteristics of saccadic eye movements in Parkinson's disease. Exp. Neurol. 31: 17–31, 1971.
 190. Mettler, F. A. Relation between pyramidal and extrapyramidal function. Res. Publ. Assoc. Res. Nerv. Ment. Dis. 21: 150–227, 1942.
 191. Mettler, F. A. Extensive unilateral cerebral removals in the primate: physiologic effects and resultant degeneration. J. Comp. Neurol. 79: 185–245, 1943.
 192. Mettler, F. A. Effects of bilateral simultaneous subcortical lesions in the primate. J. Neuropathol. Exp. Neurol. 4: 99–122, 1945.
 193. mettler, F. A., and C. C. Mettler. Labyrinthine disregard after removal of the caudate. Proc. Soc. Exp. Biol. Med. 45: 473–475, 1940.
 194. Mettler, F. A., and C. C. Mettler. Role of the neostriatum. Am. J. Physiol. 133: 594–601, 1941.
 195. Mettler, F. A., and C. C. Mettler. The effects of striatal injury. Brain 65: 242–255, 1942.
 196. Mettler, F. A., H. W. Ades, E. Lipman, and E. A. Culler. The extrapyramidal system. An experimental demonstration of function. Arch. Neurol. Psychiatry 41: 984–995, 1939.
 197. Mettler, F. A., R. L. Thompson, C. A. Houde, J. Gomex, and A. C. Dupress. The striatal syndrome. Trans. Am. Neurol. Assoc. 82: 21–31, 1957.
 198. Meyers, R. The modification of alternating tremors, rigidity, and festination of surgery of the basal ganglia. Res. Publ. Assoc. Res. Nerv. Ment. Dis. 21: 602–665, 1942.
 199. Meyers, R. The extrapyramidal system. An inquiry into the validity of the concept. Neurology 2: 627–651 1952.
 200. Meyers, R., The surgery of the hyperkinetic disorders. In: Handbook of Clinical Neurology: Diseases of the Basal Ganglia, edited by P. J. Vinken and G. W. Bruyn. Amsterdam: North‐Holland, 1968, vol. 6, p. 476–490.
 201. Meyers, R., D. B. Sweeney, and J. T. Schwidde. Hemiballismus: etiology and surgical treatment. J. Neurol. Neurosurg. Psychiatry 13: 115–126, 1950.
 202. Mones, R. J. Experimental dyskinesias in normal rhesus monkey. Adv. Neurol. 1: 665–670, 1973.
 203. Montanelli, R. P., and R. Hassler. Motor effects elicited by stimulation of the pallidothalamic system in the cat. In: Lectures on the Diencephalon, edited by W. Bergmann and J. P. Shadé. Amsterdam: Elsevier, 1964, p. 56–66.
 204. Moore, R. Y., and F. E. Bloom. Central catecholamine neuron systems: anatomy and physiology of the dopamine systems. Annu. Rev. Neurosci. 1: 129–169, 1978.
 205. Mora, F., G. F. Mogenson, and E. T. Rolls. Activity of neurons in the region of the substantia nigra during feeding in the monkey. Brain Res. 133: 267–276, 1977.
 206. Morgane, P. J. The function of the limbic and rhinic forebrain limbic midbrain systems and reticular formation in the regulation of food and water intake. Ann. NY Acad. Sci. 157: 806–848, 1969.
 207. Muakkassa, K. F., and P. L. Strick. Frontal lobe input to primate motor cortex. Soc. Neurosci. Abstr. 5: 379, 1979.
 208. Muskens, L. J. J. The central connexions of the vestibular nuclei with the corpus striatum, and their significance for ocular movements and for locomotion. Brain 45: 454–478, 1929.
 209. Nashold, B. S., Jr.. Cholinergic stimulation of globus pallidus in man. Proc. Soc. Exptl. Biol. Med. 101: 68–69, 1959.
 210. Nauta, H. J. W., and M. Cole. Efferent projections of the subthalamic nucleus. An autoradiographic study in monkey and cat. J. Comp. Neurol. 180: 1–16, 1978.
 211. Nauta, W. J. H., and U. B. Domesick. Crossroads of limbic and striatal circuitry: hypothalamo‐nigral connections. In: Limbic Mechanisms, The Continuing Evolution of the Limbic System Concept, edited by K. E. Livingston and O. Hornykiewicz. New York: Plenum, 1978, p. 75–93.
 212. Nauta, W. J. H., and W. R. Mehler. Projections of the lentiform nucleus in the monkey. Brain Res. 1: 3–42, 1966.
 213. Neafsey, E. J., C. D. Hull, and N. A. Buchwald. Preparation for movement in the cat. II. Unit activity in the basal ganglia and thalamus. Electroencephalogr. Clin. Neurophysiol. 44: 714–723, 1978.
 214. Newton, R. A., and D. D. Price. Modulation of cortical and pyramidal tract induced motor responses by electrical stimulation of the basal ganglia. Brain Res. 85: 403–422, 1975.
 215. Ng, L. K., R. E. Gelhard, T. N. Chase, and P. D. MacLean. Drug‐induced dyskinesia in monkeys: a pharmacologic model employing 6‐hydroxydopamine. Adv. Neurol. 1: 651–656, 1973.
 216. Nieuwenhuys, R., Aspects of the morphology of the striatum. In: Psychobiology of the Striatum, edited by A. R. Cools, A. H. M. Lohman, and J. H. L. Van den Bercken. Amsterdam: Elsevier, 1977, p. 1–20.
 217. Niki, H., M. Sakai, and K. Kubota. Delayed alternation performance and unit activity of the caudate head and medial orbitofrontal gyrus in the monkey. Brain Res. 38: 343–353, 1972.
 218. Oberg, R. G. E., and I. Divac. “Cognitive” functions of the neostriatum. In: The Neostriatum, edited by I. Divac and R. G. E. Oberg. Oxford: Pergamon, 1979, p. 291–314.
 219. Ohye, C., R. Bouchard, L. Larochelle, P. Bédard, R. Boucher, B. Raphy, and L. J. Poirier. Effect of dorsal rhizotomy on postural tremor in the monkey. Exp. Brain Res. 10: 140–150, 1970.
 220. Olmstead, C. E., and J. R. Villablanca. Effects of caudate nuclei or frontal cortical ablations in cats and kittens: paw usage. Exp. Neurol. 63: 559–572, 1979.
 221. Olmstead, C. E., J. R. Villablanca, R. J. Marcus, and D. L. Avery. Effects of caudate nuclei or cortex ablations in cats. IV. Bar pressing, maze learning and performance. Exp. Neurol. 53: 670–693, 1976.
 222. Olszewski, J., and D. Baxter. Cytoarchitecture of the Human Brain Stem. Philadelphia: Lippincott, 1954.
 223. Pachon, V., and P. Delmas‐Marsalet. Effets produits par l'excitation électrique des noyaux caudés chez le chien éveillé. C. R. Soc. Biol. Paris 91: 558–560, 1924.
 224. Parent, A., S. Gravel, and A. Olivier. The extrapyramidal and limbic relationship at the globus pallidus level. A comparative histochemical study in the rat, cat, and monkey. Adv. Neurol. 24: 1–11, 1979.
 225. Parent, A., L. J. Poirier, R. Boucher, and L. L. Butcher. Morphological characteristics of acetylcholinesterase‐containing neurons in the CNS of DFP‐treated monkeys. Part 2. Diencephalic and medial telencephalic structures. J. Neurol. Sci. 32: 9–28, 1977.
 226. Parkinson, J. An Essay on the Shaking Palsy. London, 1817.
 227. Parmeggiani, P. L. Sleep behavior elicited by electrical stimulation of cortical and subcortical structures in the cat. Helv. Physiol. Pharmacol. Acta 20: 347–367, 1962.
 228. Paulson, G. W. Dyskinesias in monkeys. Adv. Neurol. 1: 647–650, 1973.
 229. Peacock, S. M., Jr.. Studies on subcortical motor activity. I. Motor activity and inhibition from identical anatomical points. J. Neurophysiol. 17: 144–156, 1954.
 230. Peacock, S. M., and R. Hodes. Influences of the forebrain on somato‐motor activity. II. Facilitation. J. Comp. Neurol. 94: 409–426, 1951.
 231. Péchadre, J. C., Larochelle, L., and L. J. Poirier. Parkinsonian akinesia, rigidity and tremor in the monkey. J. Neurol. Sci. 28: 147–157, 1976.
 232. Perret, F., E. Eggenberger, and J. Siegfried. Simple and complex finger movement performance of patients with parkinsonism before and after a unilateral stereotaxic thalamotomy. J. Neurol. Neurosurg. Psychiatry 33: 16–21, 1970.
 233. Peterson, E. W., H. W. Magoun, W. S. McCulloch, and D. B. Lindsley. Production of postural tremor. J. Neurophysiol. 12: 371–384, 1949.
 234. Petras, J. M., Corticostriate and corticothalamic connections in the chimpanzee. In: Corticothalamic Projections and Sensorimotor Activities, edited by T. Frigyesi, E. Rinvik, and M. D. Yahr. New York: Raven, 1972, p. 201–219.
 235. Pijnenburg, A. J. J., and J. M. Van Rossum. Stimulation of locomotor activity following injection of dopamine into the nucleus accumbens. J. Pharm. Pharmacol. 25: 1003–1005, 1973.
 236. Poirier, L. J. Experimental and histological study of midbrain dyskinesias. J. Neurophysiol. 23: 534–551, 1960.
 237. Poirier, L. J., J. Lafleur, J. de Lean, G. Guiot, L. Larochelle, and R. Boucher. Physiopathology of the cerebellum in the monkey. 2. Motor disturbances associated with partial and complete destruction of cerebellar structures. J. Neurol. Sci. 22: 491–501, 1974.
 238. Poirier, L. J., T. L. Sourkes, G. Bouvier, T. Boucher, and S. Carabin. Striatal amines, experimental tremor and the effect of harmaline in the monkey. Brain 89: 37–52, 1966.
 239. Potegal, M., P. Copack, J. M. B. B. DeJong, G. Krauthamer, and S. Oilman. Vestibular input to the caudate nucleus. Exp. Neurol. 32: 448–465, 1971.
 240. Randrup, A., and I. Munkvad. Stereotyped activities produced by amphetamines in several animal species and man. Psychopharmacologia 11: 300–310, 1967.
 241. Ranson, S. W. Somnolence caused by hypothalamic lesions in the monkey. Arch. Neurol. Psychiatry 41: 1–25, 1939.
 242. Ranson, S. W., and C. Berry. Observations on monkeys with bilateral lesions of the globus pallidus. Arch. Neurol. Psychiatry 46: 504–508, 1941.
 243. Ranson, S. W., and M. Ranson. Pallidofugal fibers in the monkey. Arch. Neurol. Psychiatry 42: 1059–1067, 1939.
 244. Richter, R. Degeneration of the basal ganglia in monkeys from chronic carbon disulphide poisoning. J. Neuropathol. Exp. Neurol. 4: 324–353, 1945.
 245. Rolls, E. T., S. J. Thorpe, S. Maddison, A. Roer‐Hall, A. Puerto, and D. Perret. Activity of neurons in the neostriatum and related structures in the alert animal. In: The Neostriatum, edited by I. Divac and R. G. E. Oberg. Oxford: Pergamon, 1979, p. 163–182.
 246. Rougel, A. Effets inhibiteurs de la stimulation électrique du noyau caudé sur certaines catégories des movements. J. Physiol. Paris 55: 331, 1963.
 247. Rubinstein, E. H., and J. M. R. Delgado. Inhibition induced by forebrain stimulation in the monkey. Am. J. Physiol. 205: 941–948, 1963.
 248. Sasaki, K., A. Namikawa, and M. Matsunaga. Effects of stimulations of pyramidal tract and striate body upon spinal motoneurons. Jpn. J. Physiol. 10: 405–413, 1960.
 249. Sassin, J. F. Drug‐induced dyskinesia in monkey. Adv. Neurol. 10: 47–54, 1975.
 250. Sassin, J. F., S. Taub, and E. D. Weitzman. Hyperkinesia and changes in behavior produced in normal monkeys by l‐dopa. Neurology 22: 1122–1125, 1972.
 251. Schneider, P. Quantitative Analyse und Mechanismen der Bradykinesie bei Parkinsonpatienten. Dtsch. Z. Nervenheilkd. 194: 89–102, 1968.
 252. Schwab, R. S., M. E. Chafetz, and S. Walker. Control of two simultaneous voluntary motor acts in normals and in parkinsonism. Arch. Neurol. Psychiatry 72: 591–598, 1954.
 253. Schwarcz, R., and J. T. Coyle. Striatal lesions with kainic acid: neurochemical characteristics. Brain Res. 127: 235–249, 1977.
 254. Schwarz, G. A., and L. J. Barrows. Hemiballismus without involvement of Luy's body. Arch. Neurol. 2: 420–434, 1960.
 255. Sedgwick, E. M., and T. D. Williams. The response of single units in the caudate nucleus to peripheral stimulation. J. Physiol. London 189: 291–298, 1967.
 256. Segundo, J. P., and X. Machne. Unitary responses to afferent volleys in lenticular nucleus and claustrum. J. Neurophysiol. 19: 325–339, 1956.
 257. Segundo, J. P., E. F. Migliaro, and J. A. Roig. Effect of striatal and claustral stimulation upon spinal reflex and strychnine activity. J. Neurophysiol. 21: 391–399, 1958.
 258. Selby, G. Stereotaxic surgery for the relief of Parkinson's disease. Part I: A critical review. J. Neurol. Sci. 5: 315–342, 1967.
 259. Shimazu, H., T. Hongo, and K. Kubota. Two types of central influences on gamma motor system. J. Neurophysiol. 25: 309–323, 1962.
 260. Smith, M. D. Location of stereotaxic lesions confirmed at necropsy. Br. Med. J. 1: 900–906, 1968.
 261. Soltysik, S., C. D. Hull, N. A. Buchwald, and T. Fekete. Single unit activity in basal ganglia of monkeys during performance of a delayed response task. Electroencephalogr. Clin. Neurophysiol. 39: 65–78, 1975.
 262. Spiegel, E. A., H. T. Wycis, and H. Freed. Stereoencephalotomy, thalamotomy and related procedures. J. Am. Med. Assoc. 148: 446–451, 1952.
 263. Stark, L. Neurological Control Systems—Studies in Bioengineering. New York: Plenum, 1968.
 264. Stern, G. The effects of lesions in the substantia nigra. Brain 89: 449–478, 1966.
 265. Stern, J., and A. Ward. Inhibition of the muscle spindle discharge by ventrolateral thalamic stimulation. Arch. Neurol. Chicago 3: 193–204, 1960.
 266. Stern, J., and A. Ward. Supraspinal and drug modulation of the alpha motor system. Arch. Neurol. 6: 82–91, 1962.
 267. Stevens, J. R., C. Kim, P. D. MacLean. Stimulation of caudate nucleus. Arch. Neurol. Chicago 4: 47–54, 1961.
 268. Ström, G., and B. Uvnäs. Motor responses of gastrointestinal tract and bladder to topical stimulation of the frontal lobe, basal ganglia and hypothalamus in the cat. Acta Physiol. Scand. 21: 90–104, 1950.
 269. Swanson, L. W., and W. M. Cowan. A note on the connections and development of the nucleus accumbens. Brain Res. 92: 324–330, 1975.
 270. Szabo, J. Topical distribution of the striatal efferents in the monkey. Exp. Neurol. 5: 21–36, 1962.
 271. Szabo, J. The efferent projections of the putamen in the monkey. Exp. Neurol. 19: 463–476, 1967.
 272. Szabo, J. Projections from the body of the caudate nucleus in the rhesus monkey. Exp. Neurol. 27: 1–15, 1970.
 273. Szekely, E. G., A. R. Kirby, and E. A. Spiegel. The effect of stimulation of the caudate nucleus upon liver potentials. Trans. Am. Neurol. Assoc. 86: 247–249, 1961.
 274. Talland, G. A., and R. S. Schwab. Performance with multiple sets in Parkinson's disease. Neuropsychologia 2: 45–53, 1964.
 275. Tarlov, E., Synposis of current knowledge about ascending projections from the vestibular nuclei. In: The Vestibular System, edited by R. F. Naunton. New York: Academic, 1975, p. 55–69.
 276. Tatton, W. G., and R. G. Lee. Evidence for abnormal long‐loop reflexes in rigid parkinsonian patients. Brain Res. 100: 671–676, 1975.
 277. Teitelbaum, P., and A. N. Epstein. The lateral hypothalamic syndrome: recovery of feeding and drinking after lateral hypothalamic lesions. Psychol. Rev. 69: 74–90, 1962.
 278. Teuber, H.‐L. Complex functions of basal ganglia. Res. Publ. Assoc. Res. Nerv. Ment. Dis. 55: 151–169, 1976.
 279. Thach, W. T. Discharge of cerebellar neurons related to two maintained postures and two prompt movements. J. Neurophysiol. 33: 527–536, 1970.
 280. Toth, S. The role of the thalamus (VL) and pallidum in the activation of motor functions. Confin. Neurol. 32: 126–127, 1970.
 281. Travis, R. P., and D. L. Sparks. Changes in unit activity during stimuli associated with food and shock reinforcement. Physiol. Behav. 2: 171–177, 1967.
 282. Travis, R. P., and D. L. Sparks. Unitary responses and discriminative learning in the squirrel monkey: the globus pallidus. Physiol. Behav. 3: 187–196, 1968.
 283. Travis, R. P., T. F. Hooten, and D. L. Sparks. Single unit activity related to behavior motivated by food reward. Physiol. Behav. 3: 309–318, 1968.
 284. Tsukamoto, U., and F. G. Gillingham. Stereotaxic thalamotomy and l‐dopa induced involuntary movement in parkinsonism. Neurol. Med. Chir. 13: 38–45, 1973.
 285. Ungerstedt, U. Adipsia and aphagia after 6‐hydroxydopamine induced degeneration of the nigro‐striatal dopamine system. Acta Physiol. Scand. 82 (Suppl. 367): 92–122, 1971.
 286. Van Buren, J. M. Confusion and disturbance of speech from stimulation in vicinity of the head of the caudate nucleus. J. Neurosurg. 20: 148–157, 1963.
 287. Van Buren, J. M., C. L. Li, and G. A. Ojemann. The frontostriatal arrest response in man. Electroencephalogr. Clin. Neurophysiol. 21: 114–130, 1966.
 288. Vedel, J. P. Effets des stimulations du noyau caudé sur l'activité des terminaisons fusoriales primaires et secondaires du muscle soléaire. Exp. Brain Res. 22: 113–128, 1975.
 289. Vedel, J. P., and M. Coulmance. Modulation de 1'activité des terminaisons fusoriales primaires et secondaires du muscle tibial antérieur aux cours de contractions induites par stimulations du noyau caudé. Exp. Brain Res. 22: 129–144, 1975.
 290. Velasco, F., and M. Velasco. A quantitative evaluation of l‐dopa on Parkinson's disease. Neuropharmacology 12: 89–99, 1973.
 291. Villablanca, J. R., and R. J. Marcus. Is the neostriatum needed for amphetamine induced stereotyped behavior? Proc. West. Pharmacol. Soc. 17: 219–222, 1974.
 292. Villablanca, J. R., R. J. Marcus, and C. E. Olmstead. Effects of caudate nuclei or frontal cortical ablations in cats. I. Neurology and gross behavior. Exp. Neurol. 52: 389–420, 1976.
 293. Vogt, C. Quelques considérations générales à propos du syndrome du corps strié. J. Psychol. Neurol. 18: 479, 1911.
 294. Wagner, A., and K. Kalmring. The dynamic and static sensibility of the Ia afferents during electrical stimulation of the substantia nigra. Brain Res. 10: 277–280, 1968.
 295. Ward, A. A., Jr., W. S. McCulloch, and H. W. Magoun. Production of an alternating tremor at rest in monkeys. J. Neurophysiol. 11: 317–330, 1948.
 296. White, R. P., and H. E. Himwich. Circus movements and excitation of striatal and mesodiencephalic centers in rabbits. J. Neurophysiol. 20: 81–90, 1957.
 297. Whittier, J. R. Ballism and subthalamic nucleus. Arch. Neurol. Psychiatry 58: 672–692, 1947.
 298. Whittier, J. R., and F. A. Mettler. Studies of the subthalamus of the rhesus monkey. II. Hyperkinesia and other physiologic effects of subthalamic lesions with special references to the subthalamic nucleus of Luys. J. Comp. Neurol. 90: 319–372, 1949.
 299. Wiesendanger, R., M. Wiesendanger, and D. G. Ruegg. An anatomical investigation of the corticopontine projection in the primate (Macaca fascicularis and Saimiri sciureus). II. The projection from frontal and parietal association areas. Neuroscience 4: 747–765, 1979.
 300. Wilburn, M. W., and R. P. Kesner. Effects of caudate nucleus stimulation upon initiation and performance of a complex motor task. Exp. Neurol. 45: 61–71, 1974.
 301. Wilson, S. A. K. Progressive lenticular degeneration: A familial nervous disease associated with cirrhosis of the liver. Brain 34: 295–507, 1912.
 302. Wilson, S. A. K. An experimental research into the anatomy and physiology of the corpus striatum. Brain 36: 427–492, 1914.
 303. Wilson, S. A. K. Some disorders of motility and of muscle tone, with special reference to the corpus striatum. Lancet 2: 1, 53, 169, 215, 268, 1925.
 304. Wilson, S. A. K. Modern Problems in Neurology. New York: Wood, vol. 1, 1929.
 305. Winkelmüller, W. Wirkung von Reizeffekten und Ausschaltungen der Substantia nigra auf das motorische Verhalten der freibewegliche Katze. Acta Neurochir. 24: 269–303, 1971.
 306. Yeterian, E. H., and G. W. van Hoesen. Cortico‐striate projections in the rhesus monkey: the organization of certain cortico‐caudate connections. Brain Res. 139: 43–63, 1978.
 307. York, D. H. Potentiation of lumbo‐sacral reflexes by the substantia nigra. Exp. Neurol. 36: 437–448, 1972.
 308. York, D. H. Motor responses induced by stimulation of the substantia nigra. Exp. Neurol. 41: 323–330, 1973.

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Mahlon R. DeLong, Apostolos P. Georgopoulos. Motor Functions of the Basal Ganglia. Compr Physiol 2011, Supplement 2: Handbook of Physiology, The Nervous System, Motor Control: 1017-1061. First published in print 1981. doi: 10.1002/cphy.cp010221