Chapter 33 The history of movement disorders

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Abstract

Role of basal ganglia: Vesalius and Piccolomini distinguished subcortical nuclei from cortex and white matter in the 16th century. Willis' mistaken concept in the late 17th century that the corpus striatum was the seat of motor power persisted for 200 years and formed the basis of mid-19th-century localizations of movement disorders to the striatum (chorea by Broadbent and Jackson, and athetosis by Hammond). By the late 19th century, many movement disorders were described but for most no pathologic correlate was known.

Tremor: Descriptions of tremors progressed from Galen's definition in the 2nd century; to Galileo's physiologic tremor in 1610; separation of involuntary movements during action and at rest in the 17th and 18th centuries by de la Boë Sylvius and van Sweiten; description of Parkinson's disease by Parkinson, discrimination of the rest tremor of Parkinson's disease from the intention tremor of multiple sclerosis by Charcot, and recognition of familial action tremors by Dana and others in the late 19th century; and recognition of autosomal dominant essential tremor in the mid-20th century.

Parkinsonism: Pathologic changes in Parkinson's disease were recognized in the substantia nigra by Blocq and Marinescu in the late 19th century, and around 1920 Trértiakoff established Lewy bodies in the substantia nigra as a pathologic hallmark while the Vogts instead emphasized pathologic changes in the striatum; it was only in the mid-1960s that a nigrostriatal dopaminergic pathway was demonstrated and found to be critical to pathogenesis. Early treatment approaches with anticholinergic medications or crude neurosurgical ablation procedures were eclipsed in the 1960s by the advent of L-DOPA therapy due to the work of Carlsson and colleagues, Birkmayer and Hornykiewicz, Barbeau, and Cotzias. Later progress in understanding and treating Parkinson's disease included recognition of neuroleptic-induced parkinsonism beginning in the 1950s, development of dopamine agonists and elaboration of different dopamine receptors beginning in the 1960s, recognition of MPTP-induced parkinsonism in 1982 and subsequent development of experimental models of MPTP-induced parkinsonism. Since the 1980s, stereotactic neurosurgical ablation procedures such as stereotactic pallidotomy were revisited and improved, and stimulation or ablation procedures that modulate subthalamic nucleus activity were developed. Since 1990, rare genetic forms of Parkinson's disease were discovered, which accelerated progress in understanding pathogenesis, and established roles for alpha synuclein and the ubiquitin-proteasome proteolytic system. Separation of atypical forms of parkinsonism (e.g. Wilson's disease, multisystem atrophy, progressive supranuclear palsy, and corticobasal degeneration) from Parkinson's disease in the 20th century also led to important discoveries of basal ganglia function, and in the case of Wilson's disease to recognition of genetic mutations and effective treatments.

Choreoathetosis: Since the middle ages, the term chorea has been used to describe both organic and psychological disorders of motor control. Paracelcus introduced the concept of chorea as an organic medical condition in the 16th century. Sydenham's description of childhood chorea (1686) was followed by recognition in the 19th and 20th centuries that Sydenham's chorea was a manifestation of rheumatic fever; by the 1930s, rheumatic fever was recognized as a sequel of group A streptococcal pharyngitis, which could be effectively prevented with sulfonamides. Athetosis was described by Hammond (1871) and later linked by him to a malignant growth in the contralateral corpus striatum; nevertheless, athetosis has been controversial and often dismissed as a form of post-hemiplegic chorea or part of a continuum between chorea and dystonia. Huntington's classic description of adult-onset hereditary chorea (1872) was followed a century later by demonstration that Huntington's disease is caused by an unstable CAG trinucleotide repeat expansion in the Huntington disease gene on chromosome 4; this triggered a surge in research, development of various animal models, and numerous important discoveries of cell function and disease pathogenesis.

Hemiballismus and the subthalamic nucleus: The relationship between a lesion of the subthalamic nucleus of Luys and contralateral hemiballismus was first convincingly demonstrated by Martin in 1927; this led 20 years later to development of an animal model by Whittier and Mettler, who produced experimental hemichorea-hemiballismus in monkeys by lesioning the contralateral subthalamic nucleus. Since the late 1980s, the neurochemistry and neurophysiology of the subthalamic nucleus have been substantially revised with the demonstration that the subthalamic nucleus is not fundamentally inhibitory but instead provides excitatory glutaminergic inputs to the globus pallidus, and appreciation that the subthalamic nucleus serves an important role in both hyperkinetic and hypokinetic movement disorders.

Dystonia: Dystonias were often interpreted in psychological or psychiatric terms since the original descriptions of generalized dystonia by Barraquer Roviralta (1897), and familial forms of generalized primary tortion dystonia by Schwalbe (1908) and Oppenheim (1911). Although Oppenheim had first insisted that dystonia was an organic disease, it was only in the late-20th century that an organic framework was firmly established with the identification of genetic mutations in some families with dystonia and with the demonstration that the basal ganglia were often damaged contralateral to acquired hemidystonia. Focal and segmental forms of dystonia, including writer's cramp, other occupational dystonias, and torticollis, were also recognized in the 19th century. Writer's cramp was clearly described in the 1830s by Bell and Kopp, and increasingly recognized in the late 19th century due in part to Solly's influential lectures on “scriviner's palsy” in the 1860s, and to increasing prevalence because of the increase in writing using primitive writing instruments.

Myoclonus: In 1903, Lundborg proposed a classification of myoclonus that remains in use, with primary (essential), epileptic, and secondary or symptomatic categories: essential myoclonus was described by Friedrich in 1881; forms of myoclonic epilepsy were described beginning in the late 19th century by West (1861), Unverricht (1891), and Lundberg (1903); and secondary multifocal myoclonus was recognized in a wide variety of disorders beginning in the 1920s. Asterixis was described in patients with hepatic encephalopathy by Adams and Foley in 1949 and found to result from electrically silent pauses in muscle activity, which led to the concept of negative myoclonus in the 1980s. Posthypoxic action myoclonus (Lance–Adams syndrome) was described by Lance and Adams in 1963 and found to incorporate both positive and negative components.

Startle syndromes: Early descriptions of pathologic startle syndromes included Beard's description of the jumping Frenchmen of Maine (1878) and Hammond's description of miryachit (1884), both of which may have had psychological origins. In contrast, hyperekplexia or “startle disease” was described in the late 1950s and early 1960s, and genetic forms were later found to result from various mutations affecting glycinergic synapses.

Tics: Tic disorders were described by Itard (1825) and Trousseau (1873), but only gained wider recognition in the late 19th century after Charcot presented cases before his classroom audiences and after Gilles de la Tourette's classic description in 1885. Gilles de la Tourette and Charcot initially considered tic disorders and startle syndromes to be similar if not identical, but these disorders were later recognized as distinct. Psychodynamic and psychological theories or etiology gave way in the 1960s to biological theories supporting an important role for dopamine in pathogenesis, particularly with the discovery that neuroleptic medications could be useful in treatment.

Conclusion: In the last two centuries, neuroscientists and clinicians contributed greatly to our understanding of basal ganglia anatomy and physiology, as well as to movement disorder semiology, pathophysiology, treatment, and prevention. The development of animal models, and the increasing use of genetic and molecular biological techniques will lead to further advances in the coming years.

Section snippets

Distinction between cortex, white matter, and subcortical nuclei

The distinction between cortex, white matter, and subcortical nuclei was appreciated by Andreas Vesalius (1514–1564) and Francesco Piccolomini (1520–1604) in the 16th century (Vesalius, 1542, Piccolomini, 1630, Goetz et al., 2001a), and a century later British physician Thomas Willis (1621–1675) implicated the corpus striatum in motor function: “When I opened a number of cadavers of patients who had died from a long paralysis … I always found the striate bodies more softened than any other

Distinction of rest and action tremors

In the 2nd century, Galen (c. 130–200 AD) used the term tremor to refer to “involuntary alternating up-and-down motion of the limbs,” occurring during action and resulting from partial “weakness of the force that supports and moves the body” (Sider and McVaugh, 1979, Klawans et al., 1978). Galen distinguished tremor from palpitation, an “unnatural expansion and collapse” occurring at rest (Sider and McVaugh, 1979, Klawans et al., 1978). Later, in the 17th and 18th centuries, Franciscus de la

Parkinson's Disease

Parkinson's disease is of fundamental importance to the history of movement disorders, because of its common occurrence, the dramatic progress that has been made in understanding and treating the condition, and the insights this progress has provided for understanding the anatomy and function of the basal ganglia.

Encephalitis Lethargica: Von Economo's Encephalitis

In 1917 and 1918, Constantin von Economo (1876–1931) described the clinical and pathological findings of 13 cases with an unusual encephalitic condition, often with profound lethargy or stupor, that had occurred during the winter of 1916–1917 (von Economo, 1917, von Economo, 1918, von Economo, 1931):

It seems strange when sleep appears as a symptom of an illness. “Sleeping sickness” where the phenomenon of people falling asleep while eating or working was first described in two cases in our

Neuroleptic-induced parkinsonism and associated movement disorders

In the 1950s and 1960s, shortly after the introduction of chlorpromazine and other related tranquilizers (“neuroleptics”) (Delay et al., 1952, Hamon et al., 1952, Lehmann and Hanrahan, 1954), a variety of immediate and late (tardive) drug effects were recognized that included various abnormal involuntary movements, including akathisia, tremor, akinesia, parkinsonism, choreoathetosis, dystonia, and dyskinesias (Hall et al., 1956, Schonecker, 1957, Ayd, 1961, Faurbye et al., 1964). Acute

Atypical Parkinsonism

In addition to Parkinson's disease, a number of other neurodegenerative conditions have hypokinesia as a major clinical feature. Separation of these conditions from Parkinson's disease ultimately led to important anatomical and physiological discoveries concerning basal ganglia function (Goetz et al., 2001d).

Choreoathetosis

Since the Middle Ages, the term chorea (from the Greek word χoρεíα for “dance”) has been used to describe both organic and psychological disorders of motor control. In the Middle Ages, epidemics of a psychosomatic “dancing mania” erupted in central Europe coincident with the Black Plague, with St. Vitus among the various saints called upon to intercede, leading to the term “chorea Sancti Viti” (Krack, 1999, Goetz et al., 2001g). Paracelcus (1493–1541) introduced the concept of chorea as an

Dystonias

In 1944, Herz provided detailed cinematographic and electromyographic analyses of 15 personal cases of generalized dystonia, as well as an extensive review of more than 100 literature cases, and concluded that dystonic movements are best described as slow, sustained, powerful, and non-patterned contortions of the axial and appendicular muscles, with simultaneous contractions of agonist and antagonist muscles (Herz, 1944a, Herz, 1944b, Herz, 1944c). Dystonia is now defined as “a syndrome of

Myoclonus

Myoclonus is a sudden, non-suppressible, shock-like muscular contraction triggered within the central nervous system. Myoclonic movements can be “positive” or “negative”: positive myoclonus results in the contraction of a muscle or muscles, whereas negative myoclonus (e.g., asterixis) is instead associated with a brief loss of muscle tone (Schwab et al., 1951, Young and Shahani, 1986). By 1903, Lundborg proposed a classification system that remains largely in use today, with primary

Pathologic Startle Syndromes

Startle is a universal and phylogenetically ancient stereotyped reflex response to sudden, intense stimulation, which can be exaggerated in a wide variety of neuropsychiatric disorders, including various culture-bound syndromes (e.g., jumping, miryachit, and latah), hyperekplexia, startle epilepsy, benzodiazepine and alcohol withdrawal syndromes, post-traumatic stress disorder, and general anxiety disorder (Howard and Ford, 1992).

Tics

Tics are involuntary, rapid, non-rhythmic, stereotyped movements that are episodically present and occur on a background of normal movements. Tics can be categorized as motor (e.g., brief movements) or vocal (e.g., abnormal sounds produced by moving air through the nose, mouth, or throat) (The Tourette Syndrome Classification Study Group, 1993). French physician Jean Itard (1775–1838) offered the first clear description of tic disorders in 1825 (Itard, 1825), a report later cited by Gilles de

Conclusion

At the beginning of the 21st century, clinicians and neuroscientists can look with some satisfaction at the progress made in the field of movement disorders, particularly in the half century since Barbeau's historical review in 1958 (Barbeau, 1958) – for example, improved understanding of how the basal ganglia modulate cortical motor function, improved understanding of the pathophysiology of several diseases (e.g., parkinsonism, Wilson's disease, and Huntington's disease), development of

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