Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-09T19:22:01.317Z Has data issue: false hasContentIssue false

Defective Utilization of Sensory Input as the Basis for Bradykinesia, Rigidity and Decreased Movement Repertoire in Parkinson’s Disease: A Hypothesis

Published online by Cambridge University Press:  18 September 2015

M.J. Eastman
Affiliation:
Playfair Neuroscience Unit and Department of Rehabilitation Medicine, University of Toronto and Toronto Western Hospital, Toronto, Ontario
W. Bedingham
Affiliation:
Playfair Neuroscience Unit and Department of Rehabilitation Medicine, University of Toronto and Toronto Western Hospital, Toronto, Ontario
M.C. Verrier
Affiliation:
Playfair Neuroscience Unit and Department of Rehabilitation Medicine, University of Toronto and Toronto Western Hospital, Toronto, Ontario
I.C. Bruce
Affiliation:
Playfair Neuroscience Unit and Department of Rehabilitation Medicine, University of Toronto and Toronto Western Hospital, Toronto, Ontario
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

From a review of the anatomical relationships and single unit activity in the components of the basal ganglia related to limb movement, it is concluded that the major outflow from basal ganglia circuits is via the motor cortex (area 4). Recent results of recording from area 4 neurons revealed that they preferentially “encode” the higher derivatives of movement, i.e. acceleration and jerk. In the parkinsonian (PK) patient and in the monkeys treated with l-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP), EMG responses to imposed loads show a markedly increased gain of the “M2” component which depends upon the integrity of area 4 and which correlates with the severity of PK rigidity.

The above observations are considered, along with those of others (demonstrating prolonged movement times, a decreased “repertoire” of voluntary movements fractionation of voluntary movements’, inability in tracking movements without visual input, and failure to improve performance in PK’s) in relation to a model of the interactions between sensory input and motor programs. Using this model, it is hypothesized that the above PK movement deficits, as well as rigidity, can be accounted for by abnormal processing of the mechanoreceptor sensory input utilized in the generation and execution of movements. The MPTP treated monkey is suggested as a model in which to directly test the hypothesis.

Type
2. Physiology of the Basal Ganglia and Pathophysiology of Parkinson’s Disease
Copyright
Copyright © Canadian Neurological Sciences Federation 1984

References

Allum, JHJ (1976) Responses to load disturbance in human shoulder muscles: The hypothesis that one component is a pulse test information signal. Exp. Brain Res. 22: 307326.Google Scholar
Bedingham, W (1981) Input-Output Properties of the Human Wrist Reflex – A Model for Studying Neuromotor Diseases. M.Sc. Thesis, University of Toronto.Google Scholar
Bedingham, W, Tatton, WG (1983) Kinesthetic “encoding” by motor cortical neurons in the awake cat. Soc. Neurosci. Abstr. 9, 1082.Google Scholar
Bedingham, W, Tatton, WG (1984) The dependence of EMG responses evoked by imposed wrist displacements on pre-existing levels of activity in the stretched muscles. Canadian J. Neurol. Sci. (in press).CrossRefGoogle Scholar
Berardelli, A, Sabra, AF, Hallett, M (1983) Physiological mechanisms of rigidity in Parkinson’s disease. J. Neurol. Neurosurg. and Psychiat., 46: 4553.CrossRefGoogle ScholarPubMed
Burns, SR, Chiueh, CC, Markey, SP, Ebert, MH, Jacobowitz, DM, Kopin, IJ (1983) A primate model of Parkinsonism: Selective destruction of dopaminergic neurons in the pars compacta of the substantia nigra by l-methyl-4phenyl-1, 2, 3, 6-tetrahydropyridine. Proc. Nat. Acad. Sci. U.S.A. 80:45444550.CrossRefGoogle ScholarPubMed
Chan, CWY, Kearney, RE, Melvill-Jones, G (1979) Tibialis anterior response to sudden ankle displacements in normal and Parkinsonian subjects. Brain Res. 173: 303314.CrossRefGoogle ScholarPubMed
Cheney, PD, Fetz, EE (1983) Primate cortical motoneuronal cells contribute to long latency stretch reflexes. J. Physiol. (Lond.), in press.Google Scholar
Davis, GC, Williams, AC, Markey, SP, Ebert, MH, Caine, ED, Reichert, CM, Kopin, U (1979) Chronic Parkinsonism secondary to intravenous injection of meperidine analogues. Psychiat. Res. 1: 249254.CrossRefGoogle ScholarPubMed
DeLong, MR, Georgopoulos, AP (1981) Motor functions of the basal ganglia. In: Handbook of Physiology. Section I: The Nervous System. Eds. Brookhart, J.M. and Mountcastle, V.B., Vol. 2, part 2, pp. 10171061.Google Scholar
DeLong, MR, Crutcher, MD, Georgopoulos, P (1983) Relations between movement and single cell discharge in the substantia nigra of the behaving monkey. J. Neurosci. 3: 15991606.CrossRefGoogle ScholarPubMed
Evarts, EV, Teravainen, H, Beuchert, DE, Calen, DB (1979) Pathophysiology of motor performance in Parkinson’s disease. In: Dopaminergic Ergot Derivaties and Motor Functions. Ed. Fuxe, K. and Calne, D.B., London: Pergamon, pp. 4559.Google Scholar
Evarts, EV, Teravainen, H, Calne, DB (1981) Reaction time in Parkinson’s disease. Brain, 104: 167186.CrossRefGoogle ScholarPubMed
Filion, M (1979) 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: 425441.CrossRefGoogle ScholarPubMed
Flowers, K (1975) Ballistic and corrective movements in an aiming task: Intention tremor and Parkinsonian movement disorders compared. Neurol. 25:413421.CrossRefGoogle Scholar
Flowers, K (1978) Some frequency response characteristics of Parkinsonism in pursuit tracking. Brain, 101: 1934.CrossRefGoogle ScholarPubMed
Flowers, K (1976) Visual ‘closed-loop’ and ‘open-loop’ characteristics of voluntary movement in patients with Parkinsonism and intention tremor. Brain, 99: 269310.CrossRefGoogle ScholarPubMed
Georgopoulos, AP, DeLong, MR, Crutcher, MD (1983) Relations between parameters of step-tracking movements and single cell discharge in the globus pallidus and subthalamic nucleus of the behaving monkey. Neurosci. 3: 15861598.CrossRefGoogle ScholarPubMed
Gilman, S, Carr, D, Hollenberg, J (1976) Kinematic effects of deafferentation and cerebellar ablation. Brain, 99: 311330.CrossRefGoogle ScholarPubMed
Hornykiewicz, O (1963) Die Topische Lokalisation Und Verhalten Von Noradrenalin Und Dopamin (3-Hyoroxytyramin) in der Substantia Nigra Des Normalen Und Parkonsonkranken Menschen. Wien. Klin. Wschr. 75: 309312.Google Scholar
Kupfermann, I, Weiss, KR (1978) The command neuron concept. Behav. Brain Sci. I: 339.CrossRefGoogle Scholar
Lamarre, Y, Bioulac, B, Jacks, B (1978) Activity of precentral neurones in conscious monkeys: effects of deafferentiation and cerebellar ablation. J. Physiol. (Paris) 74: 253264.Google Scholar
Langston, JW, Ballard, P, Tetrud, JW, Irwin, I (1983) Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science. 219:979980.CrossRefGoogle ScholarPubMed
Lee, RG, Tatton, WG (1982) Long latency reflexes to imposed displacements of the human wrist: dependence on duration of movement. Exp. Brain Res. 45: 207216.Google ScholarPubMed
Lenz, FA, Tatton, WG, Tasker, RR (1983a) Electromyographic response to displacement of different forelimb joints in the squirrel monkey. J. Neurosci. 3: 783794.CrossRefGoogle ScholarPubMed
Lenz, FA, Tatton, WG, Tasker, RR (1983b) The effect of cortical lesions on the electromyographic response to joint displacement in the squirrel monkey forelimb. J. Neurosci. 3: 795805.CrossRefGoogle ScholarPubMed
Liles, SL (1983) Activity of neurons in the putamen associated with wrist movements in the monkey. Brain Res. 263: 156161.CrossRefGoogle ScholarPubMed
Marsden, CD, Merton, PA, Morton, HB (1972) Servo-action in human voluntary movement. Nature 238: 140143.CrossRefGoogle ScholarPubMed
Marsden, CD, Merton, PA, Morton, HB (1976) Stretch reflex and servoaction in a variety of human muscles. J. Physiol., (Lond.) 259: 531560.CrossRefGoogle Scholar
Mortimer, JA, Webster, DD (1978) Relationships between quantitative measures of rigidity and tremor and the electromyographic responses to load perturbations in unselected normal subjects and Parkinson patients. In: Progress in Clinical Neurophysiology, Vol. 4: Cerebral Motor Control in Man: Long Loop Mechanisms, ed. Desmedt, J.E., pp. 342360, Karger, Basel.Google Scholar
Mortimer, JA, Webster, DD (1979) Evidence for a quantitative association between EMG stretch responses and Parkinsonian rigidity. Brain Res. 162: 169173.CrossRefGoogle ScholarPubMed
Mountcastle, VB, Lynch, JC, Georgopoulos, A, Sakata, H and Acuna, C (1975) Posterior parietal association cortex of the monkey: command functions for the operations within extrapersonal space. J. Neurophysiol. 38: 871908.CrossRefGoogle ScholarPubMed
Pechadre, JC, Larochelle, L, Poirer, LJ (1976) Parkinsonian akinesia, rigidity and tremor in the monkey. J. Neurol. Sci. 28: 147157.CrossRefGoogle ScholarPubMed
Poirer, LJ (1960) Experimental and histological study of midbrain dyskinesia. J. Neurophysiol. 23: 534551.CrossRefGoogle Scholar
Rothwell, JC, Traub, MM, Marsden, CD (1982) Automatic and “voluntary” responses compensating for disturbances of human thumb movements. Brain 248: 3341.Google ScholarPubMed
Schultz, W (1982) Depletion of dopamine in the striatum as an experimental model of Parkinsonism: direct affects and adaptive mechanisms. Prog. Neurobiol. 18: 121166.CrossRefGoogle Scholar
Schultz, W, Ruffieux, A, Aebiseher, P (1983) The activity of pars compacta neurons of the monkey substantia nigra in relation to motor activation. Exp. Brain Res. 51: 377387.CrossRefGoogle Scholar
Taub, E, Berman, AJ (1968) Movement and learning in the absence of sensory feedback. In: The Neuropsychology of Spatially Oriented Behavior, edited by Freedman, S.J.. Homewood, IL: Dorsey, P.L.P. 174192.Google Scholar
Taub, E, Goldberg, IA, Taub, P (1975) Deafferentation in monkeys: pointing at a target without visual feedback. Exp. Neurol. 46:178186.CrossRefGoogle Scholar
Tatton, WG, Bruce, IC (1981) Comment: A schema for the interactions between motor programs and sensory input. Can. J. Physiol. Pharmacol. 59: 691699.CrossRefGoogle Scholar
Tatton, WG, Lee, RG (1975) Evidence for abnormal long-loop reflexes in Parkinsonian patients. Brain Res. 100: 671676.CrossRefGoogle ScholarPubMed
Tatton, WG, Bawa, P, Bruce, IC (1979) Altered motor cortical activity in motor cortical rigidity. In: The Extrapyramidal System, Poirier, L.J., Sourkes, T.L. and Bedard, P.J., Eds., Adv. Neurol. 10: 141160.Google Scholar
Tatton, WG, North, AGE, Bruce, IC, Bedingham, W (1983) Electromyographic and motor cortical responses to imposed displacements of the cat elbow: Disparities and homologies with those of the primate wrist. J. Neurosci. 3: 18071817.CrossRefGoogle ScholarPubMed
Tatton, WG, Bedingham, W, Verrier, MC, Blair, RDG (1984a) Characteristic alterations in the responses to imposed wrist displacement in Parkinsonian rigidity and dystonia musculorum deformans. Can. J. Neurol. Sci., In press.CrossRefGoogle Scholar
Tatton, WG, Bedingham, W, Verrier, M, Bruce, IC, Blair, RDG (1984b) Abnormalities of Mechanoreceptor-Evoked Electromyographic Activity in Central Motor Disorders. A Struppler Ed. Thieme Publishers, Stutgart, Germany. In Press.Google Scholar
Verrier, MC, Tatton, WG, Blair, RDG (1984) Characteristics of long latency responses to imposed limb displacement in cerebrovascular disease. Can. J. Neurol. Sci., In press.CrossRefGoogle Scholar
Wiesendanger, M (1981) Organization of secondary motor areas of cerebral cortex. Handbook of Physiology. Section I: The Nervous System. Eds. Brookhart, J.M. and Mountcastle, V.B. Vol. 2. Part 2, pp. 11211148.Google Scholar
Wiesendanger, M, Miles, TS (1982) Ascending pathway to low threshold muscle afferents to the cerebral cortex and its possible role in motor control, Physiol. Rev. 62: 12341270.CrossRefGoogle Scholar