Chapter 9 - Cerebellar motor syndrome from children to the elderly

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Abstract

More than a century after the description of its cardinal components, the cerebellar motor syndrome (CMS) remains a cornerstone of daily clinical ataxiology, in both children and adults. Anatomically, motor cerebellum involves lobules I–V, VI, and VIII. CMS is typically associated with errors in the metrics of voluntary movements and a lack of coordination. Symptoms and motor signs consist of speech deficits, impairments of limb movements, and abnormalities of posture/gait. Ataxic dysarthria has a typical scanning (explosive with staccato) feature, voice has a nasal character, and speech is slurred. Cerebellar mutism is most common in children and occurs after resection of a large midline cerebellar tumor. Ataxia of limbs includes at various degrees dysmetria (hypermetria: overshoot, hypometria: undershoot), dysdiadochokinesia, cerebellar tremor (action tremor, postural tremor, kinetic tremor, some forms of orthostatic tremor), isometrataxia, disorders of muscle tone (both hypotonia and cerebellar fits), and impaired check and rebound. Handwriting is irregular and some patients exhibit megalographia. Cerebellar patients show an increased body sway with a broad-based stance (ataxia of stance). Gait is irregular and staggering. Delayed learning of complex motor skills may be a prominent feature in children. CMS is currently explained by the inability of the cerebellum to handle feedback signals during slow movements and to create, store, select, and update internal models during fast movements. The cerebellum is embedded in large-scale brain networks and is essential to perform accurate motor predictions related to body dynamics and environmental stimuli. Overall, the observations in children and adults exhibiting a CMS fit with the hypothesis that the cerebellum contains neural representations reproducing the dynamic properties of body, and generates and calibrates sensorimotor predictions. Therapies aiming at a reinforcement or restoration of internal models should be implemented to cancel CMS in cerebellar ataxias. The developmental trajectory of the cerebellum, the immature motor behavior in children, and the networks implicated in CMS need to be taken into account.

Introduction

This chapter is devoted to the cerebellar motor syndrome (CMS). In the field of clinical ataxiology, CMS is a major source of disabilities in both children and adults (Holmes, 1917; Musselman et al., 2014; Manto and Mariën, 2015). CMS is typically associated with errors in the metrics of voluntary movements. The lack of coordination in voluntary movements resulting in jerky movement is one of the signatures of a cerebellar lesion (Holmes, 1917, Holmes, 1939). Symptoms and motor signs gather speech deficits, impairments of limb movements, and abnormalities of posture/gait. The vestibulocerebellar syndrome (CMS) and Schmahmann syndrome (cerebellar cognitive affective syndrome) represent the two other cornerstones of clinical ataxiology and will not be discussed here (Schmahmann and Sherman, 1998; Manto and Mariën, 2015).

Section snippets

Anatomy and physiology of the motor cerebellum

Amongst the 10 lobules of the cerebellum, lobules I–V (anterior lobe) and lobules VI and VIII (from the posterior lobe) are considered as mainly sensorimotor. Phylogenetic studies have led to the subdivision of the cerebellum into: (1) the archicerebellum, corresponding to the flocculonodular lobe (vestibulocerebellum); (2) the paleocerebellum (or spinocerebellum), which receives projections from the spinal cord via the spinocerebellar pathways; and (3) the neocerebellum, whose growth in

General rules underlying the CMS

In many cerebellar ataxias, multiple mechanisms leading to motor deficits are often combined at various degrees and explain the timecourse of symptoms (Gilman et al., 1981): reduction in blood flow (in case of stroke), edema (following a trauma), invasion of cerebellar parenchyma (especially by a tumor), inflammatory response (for instance, during cerebellitis), immune response (during an immune-mediated cerebellar ataxia).

Edema in the posterior fossa is a risk factor for obstructive

Motor ataxia: a historic perspective

The general term of ataxia was defined by Garcin (1969) as “a disturbance of coordination which, quite independently of any motor weakness, alters the direction and extent of voluntary movement and impairs the sustained voluntary or reflex muscle contractions necessary for maintaining posture and equilibrium.”

Historically, three scientists have strongly influenced our current appraisal of the deficits of limb movements in cerebellar patients (Manto, 2002):

  • 1.

    Luciani (1891) initially reported three

Control of speech

From the anatomic perspective, the hemispheric lobule VI is particularly important because it includes the lip/tongue area of a sensorimotor homunculus (Ziegler, 2016). In addition, a tongue area is also located in lobule VIII. Lobule VI receives somatosensory afferent informations from oral and facial muscles via the inferior cerebellar peduncles (Stoodley and Schmahmann, 2010). This input conveys sensory information on the sensory state of speech organs. The cerebellar hemispheres receive

Control of limb movements

Ataxia of limbs includes to varying degrees dysmetria (hypermetria: overshoot; hypometria: undershoot), dysdiadochokinesia, cerebellar tremor (action tremor, postural tremor, kinetic tremor), isometrataxia, disorders of muscle tone (both hypotonia and cerebellar fits), and impaired check and rebound.

Writing

Handwriting is irregular in cerebellar ataxias. Letters are unequal in size and are irregularly spaced (Holmes, 1917). Some patients exhibit megalographia, which is abnormally large handwriting (Frings et al., 2010). Initially, mean letter height may appear normal but repeated writing of a similar sentence is associated with an increase in the size of letters. Larger handwriting has been observed in adults with focal cerebellar disorders, in adolescents with attention deficit-hyperactivity

Myoclonus

Myoclonus consists of brief (20–200-ms) contractions (positive myoclonus) or brief cessation of muscle tone (negative myoclonus). Myoclonic jerks can be localized or generalized.

Opsoclonus-myoclonus syndrome (OMS; also called “dancing-eye syndrome” due to multidirectional conjugate eye movements) is characterized by ataxia, myoclonic jerks, and opsoclonus (Pang et al., 2009). OMS occurs typically between 12 months and 3 years of age and is associated with cerebellar atrophy, especially at the

Posture and gait

Overall, children show less efficiency for the control of posture as compared to adults. Physiologically, the upright postural sway decreases markedly from the age of 3 to 5 years, followed by a slower decline after the age of 6 years (Usui et al., 1995). In addition, under the age of 10 postural sway is higher in boys than in girls.

Both children and adults use visual, vestibular, and proprioceptive information to maintain body posture as stable as possible, but the respective contributions of

Learning of complex motor skills

Delayed learning of complex motor skills may be a prominent feature in children with cerebellar disorders. This is probably related to specific pathophysiologic mechanisms in children. In particular, motor learning is distinct in children and in adults (Patrick et al., 2014). Learning is error-driven. Prior experience and not the size of the error improves motor learning in young children. Unexpectedly, children show an immaturity in terms of motor adaptation. Adaptation of the center of

The motor phenotype in ataxic cerebral palsy

Cerebral palsy, one of the most prevalent childhood disorders which is commonly attributed to perinatal asphyxia, impacts on development and motor skills (Paneth, 2008). The motor phenotype is classically divided into spastic (increased muscle tone), dyskinetic (athetosis, dystonia), and ataxic. The ataxic phenotype accounts for only about 2% of cases (McHale et al., 2000). Motor repercussions are considerable in terms of balance and daily life activities (Grecco et al., 2017). Gait is ataxic,

CMS corresponds to pure cerebellar lesions

The CMS reported in this chapter refers to pure cerebellar lesions. However, ataxic patients may suffer from a cerebellar-plus syndrome, manifesting especially with combinations of CMS with pyramidal, extrapyramidal, sensory, or autonomic deficits. This will impact on the motor phenotype. In children, numerous genetic and developmental disorders affect simultaneously the cerebellum and extracerebellar structures, especially the brainstem. In adults, MSA and ataxic hemiparesis are two classic

Rating CMS in children and in adults

The importance of an accurate clinical quantification of CMS for the follow-up of patients is obvious. Reliable scales are available to quantify motor ataxia. Scale for the Assessment and Rating of Ataxia (SARA) is an example (Schmitz-Hübsch et al., 2006). The scale takes into account speech (0–6 points), limb movements (0–16 points), and sitting/stance/gait (0–18 points). Global score varies from 0 (no motor ataxia) to 40 (most severe ataxia). In developing children, both SARA scores and

The prevailing hypothesis to explain CMS: disruption of internal models

In numerous tasks of daily life, an integration of spatial and temporal information in the millisecond range is required (Broersen et al., 2016). The capacity of the brain to generate predictions based on spatiotemporal cues is now considered as a critical phenomenon to perform movements with the correct timing and to perform adequate perceptual judgments. Several structures in the brain cooperate to plan and execute accurate spatial and temporal motor responses, especially the cerebellum and

Acknowledgments

Mario Manto is supported by the FNRS-Belgium and the Fonds Erasme.

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