Behavioural NeurologyThe language profile of progressive supranuclear palsy
Introduction
In addition to motor symptoms, patients with Progressive Supranuclear Palsy (PSP) commonly show behavioural and cognitive disorders (Lee et al., 2016, Monza et al., 1998, Robbins et al., 1994, Soliveri et al., 2000; for a review see; Burrell, Hodges, & Rowe, 2014). The recent Movement Disorder Society (MDS) criteria (Höglinger et al., 2017) include cognitive dysfunction as one of the core diagnostic criteria, together with oculomotor dysfunction, postural instability and akinesia. Different variants have been identified, including, in addition to the classical Richardson's syndrome, initial predominance of ocular motor dysfunction, postural instability, Parkinsonism resembling idiopathic Parkinson's disease, frontal lobe cognitive or behavioural presentations, including behavioural variant frontotemporal dementia, progressive gait freezing, corticobasal syndrome, primary lateral sclerosis, cerebellar ataxia, and speech/language disorders, including nonfluent/agrammatic primary progressive aphasia (PNFA) and progressive apraxia of speech (AOS). The presence of a speech/language disorder is considered as a core clinical feature, with the highest level of diagnostic certainty in the cognitive domain (C1).
The neurolinguistic features of PSP patients presenting with an aphasic phenotype have been extensively described (Perkin et al., 1978, Esmonde et al., 1996, Sala and Spinnler, 1998, Kertesz and McMonagle, 2010, Josephs et al., 2005, Robinson et al., 2006, Boeve et al., 2003, Josephs et al., 2006, Rohrer et al., 2010). Patients with PSP-PNFA when compared with controls show an impairment in repetition, naming, semantic and phonemic fluency, single word and sentence comprehension and non-word reading (Rohrer et al., 2010, Santos-Santos et al., 2016). Connected speech in picture description is characterised by phonetic errors, reduced speech rate (Santos-Santos et al., 2016, Rohrer et al., 2010), low mean length of utterance (Santos-santos et al., 2016), and an increase in syntactic errors (Santos-Santos et al., 2016, Rohrer et al., 2010), indicating an impairment at the phonetic and syntactic levels. When PSP-PNFA is compared with non-PSP-PNFA, a more severe reduction in spontaneous speech, with fewer speech errors and less marked impairment of literacy skills were reported in the former (Rohrer et al., 2010).
Mild language disorders have been reported also in patients with the classical Richardson's syndrome. The first studies (Maher et al., 1985, Podoll et al., 1991; for a review, see; Kim & McCann, 2015) interpreted language impairment as ‘secondary to other neurological and neuropsychological disturbances’ (Podoll et al., 1991). Defective performance in lexico-semantic tasks has been successively reported by several studies (Daniele et al., 2013, Bak et al., 2005), in particular for action-verbs (vs nouns) (Bak et al., 2005; Daniele et al., 2013, Cotelli et al., 2006). More recently, an attempt to better characterize the language profile reported impairments in naming, word comprehension, semantic association and syntactic comprehension (Burrell et al., 2018). When compared to PNFA, a comparable impairment in naming, word comprehension, semantic association and syntactic comprehension tasks has been reported (Burrell et al., 2018).
In the present study, we analyse the language impairment in a sample of patients recruited from movement disorders clinics, in order to assess the prevalence of linguistic deficits and to characterize the linguistic profile in PSP patients with a primarily non-cognitive presentation. To this aim, we used a comprehensive language battery, including an analysis of a sample of connected speech obtained through a picture description task, to identify the most affected linguistic level in PSP patients presenting with different phenotypes, excluding only patients with an aphasic/speech apraxia variant. Using machine-learning algorithms, we aimed at capturing the language tests and linguistic features best describing the linguistic profile of the disorder when compared to healthy subjects. As a second aim, in order to assess the specificity of language impairment in PSP with respect to other movement disorders, we compared the performance of PSP patients with a sample of patients with Parkinson disease (PD).
Section snippets
Participants
From 2016 to 2017, fifty-nine patients were consecutively included in the study: 32 patients with a clinical diagnosis progressive supranuclear palsy (PSP) and 27 with Parkinson's disease (PD). Participants were diagnosed by experienced movement disorder neurologists, in accordance with the MDS criteria (Höglinger et al., 2017) for PSP patients and according to the UK Brain Bank Criteria (Gibb & Lees, 1988) for PD patients. Patients were recruited at the Movement Disorders Center of the
Neuropsychological assessment
The percentage of PSP and PD impaired on each test, on the basis of normative data, as well as the means of the corrected scores (and the p values for differences) for both patient groups are reported in Table 1S in the Supplementary Materials. A high percentage of PSP patients showed an impairment in several cognitive domains, including attentional-executive, visuo-constructional abilities, orofacial praxis and immediate recall tasks, with a mean score significantly lower than PD patients.
Speech and language assessment
Discussion
The aim of this study is to identify the linguistic profile of PSP patients presenting primarily with a movement disorder, through a comprehensive assessment including language tests and the linguistic features provided by connected speech analysis.
The first result is that subtle language deficits can be observed also in PSP patients with non aphasic/speech apraxia presentation. Machine learning classifications, using separately language tests and linguistic features, resulted in a high
Conclusion
We have demonstrated high classification accuracy provided by machine learning in discriminating PSP from healthy subjects and PSP from PD, in particular combining language tests and linguistic features provided by a connected speech task. Although PSP with prevalent movement disorders is not typically associated with language deficits, our analyses indicate the presence of a subtle language impairment, involving mainly lexical-semantic and discourse-pragmatic levels. While lexical-semantic
Competing interests
None declared.
Acknowledgements
This study was supported by the MRC Research Grant: Ref MR/N025881/1, and by the “AIRAlzh Onlus” and “ANCC-COOP” Italia issued to V.M. Borsa.
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