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10 - Paradoxes in Parkinson's disease and other movement disorders

Published online by Cambridge University Press:  05 December 2011

By
Ashwani Jha  and
Peter Brown
Edited by
Narinder Kapur
With
Alvaro Pascual-Leone ,
Vilayanur Ramachandran ,
Jonathan Cole ,
Sergio Della Sala ,
Tom Manly  and
Andrew Mayes
Foreword by
Oliver Sacks
Ashwani Jha
Affiliation:
Institute of Neurology
Peter Brown
Affiliation:
Institute of Neurology
Narinder Kapur
Affiliation:
University College London
Alvaro Pascual-Leone
Affiliation:
Harvard Medical School
Vilayanur Ramachandran
Affiliation:
University of California, San Diego
Jonathan Cole
Affiliation:
University of Bournemouth
Sergio Della Sala
Affiliation:
University of Edinburgh
Tom Manly
Affiliation:
MRC Cognition and Brain Sciences Unit
Andrew Mayes
Affiliation:
University of Manchester
Oliver Sacks
Affiliation:
Columbia University Medical Center
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Summary

Summary

The phenomenon of paradoxical facilitation has its greatest clinical impact in the field of movement disorders. Tens of thousands of people suffering from Parkinson's disease have spectacularly improved thanks to precisely placed surgical lesions or electrical stimulation deep in the centre of the brain. This chapter reports how this paradoxical benefit has driven science and medicine to unravel some of the secrets of one of the most complex circuits in the brain – the basal ganglia. We describe how careful anatomical studies of the basal ganglia have exposed their underlying circuitry, allowing scientists to ascribe function and capture dysfunction in disease. Against this background, we set a number of clinical paradoxes that challenge this model. These force us to take a leap in our conceptualization of the brain, considering it as a plastic network, perturbed by one or more disruptive signals in disease.

Meyers' observation – the paradox

As a young neurosurgeon in the Brooklyn Hospital, New York, Russell Meyers was inspired by an anecdote from his supervisor E. Jefferson Browder. Whilst performing a frontal lobectomy (presumably to remove a tumour), Browder had to extend the lesion far back into an unaffected area deep in the centre of the brain known as the basal ganglia. Coincidentally this patient also had early signs similar to Parkinson's disease, a degenerative condition causing slow, stiff movement and shaking. When the patient awoke after surgery, Browder noted something very unexpected. The patient's Parkinsonian symptoms had disappeared, completely (Meyers,1940; Clower, 2002).

Type
Chapter
Information
The Paradoxical Brain , pp. 189 - 203
Publisher: Cambridge University Press
Print publication year: 2011

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References

Albin, R. L., Young, A. B., & Penney, J. B. (1989). The functional anatomy of basal ganglia disorders. Trends in Neuroscience, 12: 366–75.CrossRefGoogle ScholarPubMed
Alexander, G. E., Delong, M. R., & Strick, P. L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience, 9: 357–81.CrossRefGoogle ScholarPubMed
Alonso-Frech, F., Zamarbide, I., Alegre, M., et al. (2006). Slow oscillatory activity and levodopa-induced dyskinesias in Parkinson's disease. Brain, 129: 1748–57.CrossRefGoogle ScholarPubMed
Androulidakis, A., Doyle, L., Yarrow, K., Litvak, V., Gilbertson, T., & , P., B. (2007a). Anticipatory changes in beta synchrony in the human corticospinal system and associated improvements in task performance. European Journal of Neuroscience, 25: 3758–65.CrossRefGoogle ScholarPubMed
Androulidakis, A. G., Kuhn, A. A., Chen, C. C., et al. (2007b). Dopaminergic therapy promotes lateralized motor activity in the subthalamic area in Parkinson's disease. Brain, 130: 457–68.CrossRefGoogle ScholarPubMed
Asmus, F., Huber, H., Gasser, T., & Schols, L. (2008). Kick and rush: paradoxical kinesia in Parkinson disease. Neurology, 71: 695.CrossRefGoogle ScholarPubMed
Barbaud, A., Hadjout, K., Blard, J. M., & Pages, M. (2001). Improvement in essential tremor after pure sensory stroke due to thalamic infarction. European Neurology, 46: 57–9.CrossRefGoogle ScholarPubMed
Benabid, A. L., Pollak, P., Louveau, A., Henry, S., & Rougemont, J. (1987). Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Applied Neurophysiology, 50: 344–6.Google ScholarPubMed
Bergman, H., Wichmann, T., Karmon, B., & Delong, M. R. (1994). The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. Journal of Neurophysiology, 72: 507–20.CrossRefGoogle ScholarPubMed
Bhatia, K. P., & Marsden, C. D. (1994). The behavioural and motor consequences of focal lesions of the basal ganglia in man. Brain, 117: 859–76.CrossRefGoogle ScholarPubMed
Bland, B. H., & Oddie, S. D. (2001). Theta band oscillation and synchrony in the hippocampal formation and associated structures: the case for its role in sensorimotor integration. Behaviour and Brain Research, 127: 119–36.CrossRefGoogle ScholarPubMed
Brown, P., & Eusebio, A. (2008). Paradoxes of functional neurosurgery: clues from basal ganglia recordings. Movement Disorders, 23: 12–20.CrossRefGoogle ScholarPubMed
Brown, P., Chen, C. C., Wang, S., et al. (2006). Involvement of human basal ganglia in offline feedback control of voluntary movement. Current Biology, 16: 2129–34.CrossRefGoogle ScholarPubMed
Chen, C. C., Brucke, C., Kempf, F., et al. (2006a). Deep brain stimulation of the subthalamic nucleus: a two-edged sword. Current Biology, 16: R952–3.CrossRefGoogle ScholarPubMed
Chen, C. C., Kuhn, A. A., Hoffmann, K. T., et al. (2006b). Oscillatory pallidal local field potential activity correlates with involuntary EMG in dystonia. Neurology, 66: 418–20.CrossRefGoogle ScholarPubMed
Chen, C. C., Litvak, V., Gilbertson, T. G., et al. (2007). Excessive synchronisation of basal ganglia neurons at 20 Hz slows movement in Parkinson's disease. Experimental Neurology, 205: 214–21.CrossRefGoogle Scholar
Choi, S. M., Lee, S. H., Park, M. S., Kim, B. C., Kim, M. K., & Cho, K. H. (2008). Disappearance of resting tremor after thalamic stroke involving the territory of the tuberothalamic artery. Parkinsonism Related Disorders, 14: 373–5.CrossRefGoogle ScholarPubMed
Clower, W. (2002). Lesions as therapy: surgical intervention in Parkinson's Disease prior to L-Dopa. Journal of the History of the Neurosciences, 11: 375–91.CrossRefGoogle ScholarPubMed
Constantino, A. E., & Louis, E. D. (2003). Unilateral disappearance of essential tremor after cerebral hemispheric infarct. Journal of Neurology, 250: 354–5.CrossRefGoogle ScholarPubMed
Costa, R. M., Lin, S. C., Sotnikova, T. D., et al. (2006). Rapid alterations in corticostriatal ensemble coordination during acute dopamine-dependent motor dysfunction. Neuron, 52: 359–69.CrossRefGoogle ScholarPubMed
Cock, V. C., Vidailhet, M., Leu, S., et al. (2007). Restoration of normal motor control in Parkinson's disease during REM sleep. Brain, 130: 450–6.CrossRefGoogle ScholarPubMed
Decoteau, W. E., Thorn, C., Gibson, D. J., et al. (2007). Learning-related coordination of striatal and hippocampal theta rhythms during acquisition of a procedural maze task. Proceedings of the National Academy of Sciences of the United States of America, 104: 5644–9.CrossRefGoogle ScholarPubMed
Delong, M. R. (1990). Primate models of movement disorders of basal ganglia origin. Trends in Neuroscience, 13: 281–5.CrossRefGoogle ScholarPubMed
Doyle, L. M., Kuhn, A. A., Hariz, M., Kupsch, A., Schneider, G. H., & Brown, P. (2005). Levodopa-induced modulation of subthalamic beta oscillations during self-paced movements in patients with Parkinson's disease. European Journal of Neuroscience, 21: 1403–12.CrossRefGoogle ScholarPubMed
Fogelson, N., Williams, D., Tijssen, M., Bruggen, G., Speelman, H., & Brown, P. (2006). Different functional loops between cerebral cortex and the subthalmic area in Parkinson's disease. Cerebral Cortex, 16: 64–75.CrossRefGoogle ScholarPubMed
Foncke, E. M., Bour, L. J., Speelman, J. D., Koelman, J. H., & Tijssen, M. A. (2007). Local field potentials and oscillatory activity of the internal globus pallidus in myoclonus-dystonia. Movement Disorders, 22: 369–76.CrossRefGoogle ScholarPubMed
Frank, M. J., Samanta, J., Moustafa, A. A., & Sherman, S. J. (2007). Hold your horses: impulsivity, deep brain stimulation, and medication in Parkinsonism. Science, 318: 1309–12.CrossRefGoogle ScholarPubMed
Gengler, S., Mallot, H. A., & Holscher, C. (2005). Inactivation of the rat dorsal striatum impairs performance in spatial tasks and alters hippocampal theta in the freely moving rat. Behaviour and Brain Research, 164: 73–82.CrossRefGoogle ScholarPubMed
Gilbertson, T., Lalo, E., Doyle, L., Di Lazzaro, V., Cioni, B., & Brown, P. (2005). Existing motor state is favored at the expense of new movement during 13–35 Hz oscillatory synchrony in the human corticospinal system. Journal of Neuroscience, 25: 7771–9.CrossRefGoogle ScholarPubMed
Guehl, D., Dehail, P., Seze, M. P., et al. (2006). Evolution of postural stability after subthalamic nucleus stimulation in Parkinson's disease: a combined clinical and posturometric study. Experimental Brain Research, 170: 206–15.CrossRefGoogle ScholarPubMed
Hammond, C., Bergman, H., & Brown, P. (2007). Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends in Neuroscience, 30: 357–64.CrossRefGoogle ScholarPubMed
Kim, D. H., Kim, J., Kim, J. M., & Lee, A. Y. (2006a). Disappearance of writing tremor after striatal infarction. Neurology, 67: 362–3.CrossRefGoogle ScholarPubMed
Kim, J. S., Park, J. W., Kim, W. J., Kim, H. T., Kim, Y. I., & Lee, K. S. (2006b). Disappearance of essential tremor after frontal cortical infarct. Movement Disorders, 21: 1284–5.CrossRefGoogle ScholarPubMed
Kuhn, A. A., Kupsch, A., Schneider, G. H., & Brown, P. (2006). Reduction in subthalamic 8–35 Hz oscillatory activity correlates with clinical improvement in Parkinson's disease. European Journal of Neuroscience, 23: 1956–60.CrossRefGoogle ScholarPubMed
Liu, X., Griffin, I. C., Parkin, S. G., et al. (2002). Involvement of the medial pallidum in focal myoclonic dystonia: a clinical and neurophysiological case study. Movement Disorders, 17: 346–53.CrossRefGoogle ScholarPubMed
Marsden, C. D., & Obeso, J. A. (1994). The functions of the basal ganglia and the paradox of stereotaxic surgery in Parkinson's disease. Brain, 117: 877–97.CrossRefGoogle ScholarPubMed
Maurer, C., Mergner, T., Xie, J., Faist, M., Pollak, P., & Lucking, C. H. (2003). Effect of chronic bilateral subthalamic nucleus (STN) stimulation on postural control in Parkinson's disease. Brain, 126: 1146–63.CrossRefGoogle ScholarPubMed
McIntyre, C. C., & Hahn, P. J. (2010). Network perspectives on the mechanisms of deep brain stimulation. Neurobiology of Disease, 38: 329–37.CrossRefGoogle ScholarPubMed
Meyers, R. (1940). Surgical proceedure for the postencephalitic tremor, with notes on the physiology of premotor fibres. Archives of Neurology and Psychiatry, 44: 455–7.Google Scholar
Nachev, P., Wydell, H., O'Neill, K., Husain, M., & Kennard, C. (2007). The role of the pre-supplementary motor area in the control of action. National Review of Neuroscience, 11: 856–69.Google Scholar
Nagaratnam, N., & Kalasabail, G. (1997). Contralateral abolition of essential tremor following a pontine stroke. Journal of Neurological Science, 149: 195–6.CrossRefGoogle ScholarPubMed
Nakashima, K., Takahashi, K., & Ota, M. (1993). Cessation of writer's cramp after stroke. Movement Disorders, 8: 249–51.CrossRefGoogle ScholarPubMed
Owen, A. M. (2004). Cognitive dysfunction in Parkinson's disease: the role of frontostriatal circuitry. Neuroscientist, 10: 525–37.CrossRefGoogle ScholarPubMed
Piccolo, I., Defanti, C. A., Soliveri, P., Volonte, M. A., Cislaghi, G., & Girotti, F. (2003). Cause and course in a series of patients with sporadic chorea. Journal of Neurology, 250: 429–35.CrossRefGoogle Scholar
Pinto, S., Gentil, M., Krack, P., et al. (2005). Changes induced by levodopa and subthalamic nucleus stimulation on parkinsonian speech. Movement Disorders, 20: 1507–15.CrossRefGoogle ScholarPubMed
Probst-Cousin, S., Druschky, A., & Neundorfer, B. (2003). Disappearance of resting tremor after ‘stereotaxic’ thalamic stroke. Neurology, 61: 1013–4.CrossRefGoogle ScholarPubMed
Redgrave, P., Prescott, T. J., & Gurney, K. (1999). The basal ganglia: a vertebrate solution to the selection problem?Neuroscience, 89: 1009–23.CrossRefGoogle ScholarPubMed
Rezai, A. R., Machado, A. G., Deogaonkar, M., Azmi, H., Kubu, C., & Boulis, N. M. (2008). Surgery for movement disorders. Neurosurgery, 62(Suppl 2): 809–38.CrossRefGoogle ScholarPubMed
Rivlin-Etzion, M., Marmor, O., Heimer, G., Raz, A., Nini, A., & Bergman, H. (2006). Basal ganglia oscillations and pathophysiology of movement disorders. Current Opinions in Neurobiology, 16: 629–37.CrossRefGoogle ScholarPubMed
Robottom, B. J., Weiner, W. J., Asmus, F., Huber, H., Gasser, T., & Schols, L. (2009). Kick and rush: paradoxical kinesia in Parkinson disease. Neurology, 73: 328; author reply 328–9.CrossRefGoogle ScholarPubMed
Rodriguez-Oroz, M. C., Obeso, J. A., Lang, A. E., et al. (2005). Bilateral deep brain stimulation in Parkinson's disease: a multicentre study with 4 years follow-up. Brain, 128: 2240–9.CrossRefGoogle ScholarPubMed
Saint-Cyr, J. A., Trepanier, L. L., Kumar, R., Lozano, A. M., & Lang, A. E. (2000). Neuropsychological consequences of chronic bilateral stimulation of the subthalamic nucleus in Parkinson's disease. Brain, 123: 2091–108.CrossRefGoogle ScholarPubMed
Schlesinger, I., Erikh, I., & Yarnitsky, D. (2007). Paradoxical kinesia at war. Movement Disorders, 22: 2394–7.CrossRefGoogle ScholarPubMed
Silberstein, P., Kuhn, A. A., Kupsch, A., et al. (2003). Patterning of globus pallidus local field potentials differs between Parkinson's disease and dystonia. Brain, 126: 2597–608.CrossRefGoogle ScholarPubMed
Silberstein, P., Pogosyan, A., Kuhn, A. A., et al. (2005). Cortico-cortical coupling in Parkinson's disease and its modulation by therapy. Brain, 128: 1277–91.CrossRefGoogle ScholarPubMed
Smeding, H. M., Speelman, J. D., Koning-Haanstra, M., et al. (2006). Neuropsychological effects of bilateral STN stimulation in Parkinson disease: a controlled study. Neurology, 66: 1830–6.CrossRefGoogle ScholarPubMed
Souques, M. (1921). Rapport sur les syndrome parkinsoniens. Séance du 3–4 Juin 1921. Review of Neurology, 1: 534.Google Scholar
Spiegel, E. A., Wycis, H. T., Marks, M., & Lee, A. J. (1947). Stereotaxic apparatus for operations on the human brain. Science, 106: 349–50.CrossRefGoogle ScholarPubMed
Tang, J. K., Mahant, N., Cunic, D., et al. (2007). Changes in cortical and pallidal oscillatory activity during the execution of a sensory trick in patients with cervical dystonia. Experimental Neurology, 204: 845–8.CrossRefGoogle ScholarPubMed
Valls-Sole, J., Rothwell, J. C., Goulart, F., Cossu, G., & Munoz, E. (1999). Patterned ballistic movements triggered by a startle in healthy humans. Journal of Physiology, 516: 931–8.CrossRefGoogle ScholarPubMed
Voon, V., Potenza, M. N., & Thomsen, T. (2007). Medication-related impulse control and repetitive behaviors in Parkinson's disease. Current Opinions in Neurology, 20: 484–92.CrossRefGoogle ScholarPubMed
Wilson, S. (1925). Disorders of motility and of muscle tone, with special reference to the corpus striatum. Lancet, 2: 1–10, 53–62, 169–78, 215–19, 268–76.Google Scholar

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