Apraxia of speech and cerebellar mutism syndrome: a case report

Cerebellar mutism syndrome (CMS) or posterior fossa syndrome (PFS) is characterized by a transient period of cerebellar mutism combined with a range of neurological (motor) disturbances, neuropsychological (cognitive, affective/behavioral) abnormalities and neurogenic speech/language deficits. It is most commonly observed in children and has only been occasionally reported in adults [1–4]. CMS is typically associated with posterior fossa tumor surgery [2], but traumatic brain injury [5], stroke [2, 6] and infections [7, 8] may also cause this syndrome. In a review of 257 children who developed CMS after surgery [9] 62.7% of the cases had a medulloblastoma, 24.9% an astrocytoma, 11.2% an ependymoma, 0.4% a meningioma (ME), 0.4% a germinoma, and 0.4% germ cells. The symptoms of CMS are linked to damage to various parts of the cerebellum and the cerebello-cerebral pathways passing through the brainstem [10]. Immediately after surgery, most patients who later develop CM present ataxia and dysmetria. After a linguistically symptom free interval of some days (generally 1 and a half to 2 days) the patients become mute [9]. Onset of CM is typically accompanied by additional neurological signs and affective/behavioral disorders. Neurological symptoms may consist of oculomotor and oral motor dysfunction, hypotonia, ataxia, paresis, dysmetria, incontinence, tremor and 6th and 7th cranial nerve palsies [11, 12]. Affective/behavioral disorders include irritability and whining (2/3) and apathy (1/2) and tend to resolve before remission of CM [13, 14]. After a period of CM (mean time: 47.6 days/43 days) [9, 15], speech slowly returns and is often characterized by distorted vowels, slowed speech, prolonged phonemes, monopitch/monoloudness, hypernasality, vocal tremor and dysarthria [13, 15–19]. Dysarthria which characterizes motor speech in most of the children after remission of mutism (98.8%) [15, 20] is typically defined as ataxic dysarthria [20]. Only a handful of studies reported that patients affected by CM had non-motor language problems such as a reduced verbal output with short phrases, wordfinding difficulties and disruption of grammar [14, 20, 21]. Neuropsychological studies revealed a range of executive dysfunctions, visuospatial problems and a general intellectual decline during longitudinal follow-up (even 1 year postsurgery) [20, 22]. The residual complex of cognitive, linguistic and affective symptoms in pediatric posterior fossa tumor patients are consistent with the Cerebellar Cognitive Affective Syndrome (CCAS) or Schmahmann’s syndrome [21, 23–25]. Schmahmann’s syndrome consists of a cluster of neuropsychological and affective impairments but do not per se include motor symptoms or CM [26]. However, it might be argued that CM represents the extreme end of adynamic speech on a fluency/dysfluency continuum, which forms part of the linguistic cluster of Schmahmann’s syndrome.

The pathophysiological mechanisms subserving CMS remain to be clarified. The immediate onset of ataxia and dysmetria are likely due to surgical impact on the cerebellum. Secondary processes initiated by the tumor resection seem to play a role in the delayed onset of symptoms [11, 27] and may involve edema of the cerebellum and the cerebellar peduncles, hypoperfusion and subsequent ischemia of the cerebellum, transient dysregulation of neurotransmitter release, crossed cerebello-cerebral diaschisis, and axonal injury. Diaschisis affecting supratentorial brain areas may indeed explain some cognitive symptoms of CMS. Mariën et al. [28] showed that lesions of the right cerebellar hemisphere may result in functional deactivation of supratentorial language areas in the left cerebral hemisphere, and introduced the concept of a ‘lateralized linguistic cerebellum’. Hypoperfusion in frontal regions due to cerebellar lesions may lead to grammatical and executive disorders [29]. SPECT (Single-Photon Emission Computed Tomography) studies have shown hypoperfusion in dominant or bilateral frontal regions during mutism and improvement in blood flow when speech returned [20, 28].

Following remission of CM the cluster of motor speech characteristics are often defined as ataxic dysarthria, since this type of dysarthria is typically found in a context of cerebellar pathology [29]. However, there is no clear-cut typology, which unambiguously classifies the motor speech symptoms as ataxic dysarthria. In an auditory-perceptual analysis of the speech characteristics of 24 children and adolescents, De Smet et al. [16] showed that typical ataxic speech characteristics such as imprecise consonants, excess and equal stress, and irregular articulatory breakdown were only present in a minority of the patients (fewer than 25%). Distorted vowels not associated with irregular articulatory breakdown and/or excess and equal stress were found in seven of the 13 (54%) patients, which confirms that this speech characteristic per se is not distinctive of ataxic dysarthria. As a result, the exact nature of motor speech pathology of CMS remains to be elucidated.

This study investigates the speech and language symptoms following posterior fossa medulloblastoma surgery in a 12-year-old right-handed boy. A detailed description of the motor speech characteristics may help to unravel the puzzling nature and pathophysiology of the CMS.

This patient with CMS not only shares a number of overt similarities but also some differences with the complex of symptoms that constitute CMS as generally described in the literature. As in most cases with CMS, this patient developed cerebellar mutism (CM) combined with neurological symptoms, neuropsychological disturbances and speech deficits following posterior fossa tumor surgery [1–4]. Postoperatively, a spectrum of neurological symptoms were found that consisted of: ataxia, dysmetria, hypotonia, akinesia, diplopia (trochlear and abducens paresis) and a bilateral paresis which affected the right body-side more prominently. The boy became mute 4 days after partial resection of a medulloblastoma in the posterior fossa. During these first 4 days after surgery, reduced verbal output and a general state of apathy were found. The onset of CM was accompanied by apraxic deficits (oral and eyelid apraxia) as well as affective and behavioral disturbances (emotional instability, infantile behavior, irritability). After 4 weeks of CM, speech slowly returned. Although behavioral and affective symptoms diminished, infantile behavior persisted. At 6 weeks postsurgery, formal assessment of speech (DIAS) was consistent with a diagnosis of AoS. Ataxic dysarthria was formally excluded since no vowel distortions, imprecise consonant production, excess and equal stress and irregular articulatory breakdown were found. The neurolinguistic work-up further showed distorted language production and perception, wordfinding difficulties, grammatical disturbances and verbal fluency deficits. After 6 months, speech and language as well as motor skills improved but did not return to preoperative level.

Although the neurological and neuropsychological (affective, cognitive) symptoms of this patient are typical for CMS [13–20, 22], speech and language symptoms were markedly different from what is typically described in the literature [20]. Non-motor language deficits are only rarely reported in the CMS literature. Indeed, after a careful review of 167 cases published between 1972 and 2006, De Smet et al. [15] identified 165 (98.8%) patients with postoperative motor speech disorders and only a handful of cases with non-motor language deficits [38]. The language deficits described in the study of Riva and Georgi [38] consisted of agrammatic, hypospontaneous language. However, language symptoms in the CMS population have not been systematically investigated by means of formal instruments and might therefore have been overlooked [28]. In this patient syntactic, wordfinding and verbal fluency deficits were identified as the most prominent language deficits. Only two studies similarly described language deficits following posterior fossa tumor surgery. In the study of De Smet et al. [20] 4 patients affected by CM suffered from adynamic speech production, impaired verbal fluency, word-finding difficulties and grammatical disturbances at 1.5–6 months postoperatively. Levisohn et al. [21] showed that 11 out of 19 posterior fossa tumor patients (regardless of the presence/absence of CM) had word-finding difficulties/severe language problems within 2 years from surgery. The linguistic symptoms seem to form part of the Cerebellar Cognitive Affective Syndrome (CCAS) or Schmahmann’s syndrome [21, 23–25] that refers to a constellation of neuropsychological (visuo-spatial, executive), affective and linguistic impairments that are caused by cerebellar lesions. PFS, CM, CCAS are related conditions that have been used interchangeable in studies, which makes it hard to compare the results of different studies.

In the posterior fossa literature motor speech symptoms following CM are typically defined as ataxic dysarthria in posterior fossa literature [13, 15–19]. Reviewing the data on 283 childhood cases to chart the mode of recovery of motor speech production after CMS, De Smet et al. [20] showed that 98.8% of the reviewed cases displayed motor speech impairments. However, perceptual speech analysis in 24 children and adolescents (of whom 12 developed CMS) disclosed that the most prominent speech deficits consisted of distorted vowels, slow rate, voice tremor, and monopitch and that typical ataxic speech characteristics such as imprecise consonants, excess and equal stress, and irregular articulatory breakdown were only present in half of the patients (54%) [16]. De Smet et al. [16] concluded that motor speech disturbances following cerebellar tumor surgery do not necessarily resemble ataxic dysarthria. Acoustic/phonetic speech analyses and DIAS assessment [33] in this patient revealed the following characteristics: high pitch (falsetto voice), dental articulatory setting, hypernasality, prolongation of phonemes, slowed/staccato speech, devoicing of consonants, frequent self-corrections, seeking behavior/articulatory groping, initiation problems, syllable segmentations, cluster segmentations, worse performance for alternating sequences than for sequential sequences and an articulation complexity effect. Although hypernasality, prolongation of phonemes and slowed staccato speech are symptoms that overlap between ataxic dysarthria and AoS, there is ample evidence to conclude that this patient’s deviant speech production is consistent with AoS in the absence of ataxic dysarthria [29, 39]. First, DIAS results clearly matched a typological diagnosis of AoS as six out of the eight typical AoS features were met (seeking behavior/articulatory groping, initiation problems, syllable segmentations, cluster segmentations, worse performance for alternating sequences than for sequential sequences and an articulation complexity effect). Second, patients with AoS typically have problems with irregular voicing or devoicing [40] and frequently correct themselves [41], which was also the case in this patient (devoicing of consonants, self-corrections). Third, the three most typical symptoms of ataxic speech (i.e. imprecise consonants, excess and equal stress and irregular articulatory breakdown) were not observed in this patient. The origin of the high pitch falsetto voice and dental articulatory setting are unclear. These symptoms are neither typical of AoS nor of ataxic dysarthria. Tumor surgery may cause vagal neuropathy and as such vocal fold paralysis [42] inducing a compensatory falsetto or paralytic falsetto [43, 44]. However, ENT (ear, nose, throat) investigations did not reveal vagal neuropathy or vocal fold paralysis. The falsetto voice and the dental articulatory setting might therefore reflect phenomena linked to the childish/infantile behavior of this patient.

As a result it is hypothesized that the CM in this patient was more likely induced by an underlying speech planning and organization deficit (apraxia) and not by a pure motor disorder (dysarthria). AoS and ataxic dysarthria share some semiological similarities (e.g. irregularity, slowness), but these may reflect more universal aspects (e.g. motor slowness) [29]. The role of the cerebellum in ataxic dysarthria is generally acknowledged [45], whereas a possible role of the cerebellum in AoS remains to be elucidated. According to Ziegler [29] cerebellar lesions are not implicated in the origin of AoS. The primary lesion sites that have been assigned to AoS are Brodmann area 44 of Broca’s area, the left inferior premotor and motor cortex, and the left anterior insular cortex [46–48]. However, the aforementioned clinical symptoms of this case’s speech clearly match with the concepts of AoS put forward by Ziegler [29]: inconsistent speech movement aberrations resulting in inconsistent sound distortions and phonemic errors, slowed speech, breakdown of speech rhythm due to groping false starts, inter-/intrasyllable pauses, scanned rhythm, frequent self-correction. Consequently, in this case AoS was formally diagnosed and related to the cerebellar lesion. In addition, functional neuroimaging and clinical studies have recently shown that the cerebellum is also involved in speech motor control, which is required for the planning and execution of speech [49–52]. Nevertheless the exact role of the cerebellum in motor planning versus motor execution of speech is still unclear [29, 53]. Whether the cerebellum has a direct or indirect role in the motor speech planning network might be further investigated using SPECT reflecting distant functional effects in anatomically connected cerebral regions primarily involved in motor speech planning such as Broca's area, the language dominant inferior premotor and motor cortex and the anterior insula [46–48].

This case might be the first example that clearly demonstrates AoS following posterior fossa tumor surgery. Therefore, the findings add to the view that the cerebellum plays a crucial role in the planning and execution of speech. Whether the cerebellum has a direct or indirect role in motor speech planning needs to be further investigated. Although residual speech symptoms following CMS are frequently defined as ataxic dysarthria, there is no consensus on the core speech characteristics that follow CM [9, 12, 16, 54, 55]. Therefore, this case presenting apraxic rather than dysarthric speech deficits provides novel evidence that might add to current insights in the core features of motor speech and language disturbances in CMS.

CMS consists of a constellation of neuropsychiatric, neuropsychological and neurogenic speech and language deficits. It is most commonly observed in children after posterior fossa tumor surgery. The most prominent feature of CMS is mutism, which generally starts after a few days after the operation, has a limited duration and is typically followed by motor speech deficits. On the pathophysiolgical level the complex range of symptoms unambiguously reflects crucial involvement of the cerebellum and the cerebro-cerebellar pathways in disrupted cognitive and affective processes. However, the core speech characteristics of CMS and the exact role of the cerebellum in motor speech planning versus execution are still unclear. In this article, a detailed description is provided of the motor speech and language deficits following posterior fossa tumor surgery in a 12-year-old right-handed boy. In-depth analyses of motor speech production revealed features consistent with a diagnosis of AoS while ataxic dysarthria was absent. Future research is needed to confirm these findings and to explore the precise role of the cerebellum in motor speech planning processes.