Connected speech production in three variants of primary progressive aphasia

Abstract

Primary progressive aphasia is a clinical syndrome defined by progressive deficits isolated to speech and/or language, and can be classified into non-fluent, semantic and logopenic variants based on motor speech, linguistic and cognitive features. The connected speech of patients with primary progressive aphasia has often been dichotomized simply as 'fluent' or 'non-fluent', however fluency is a multidimensional construct that encompasses features such as speech rate, phrase length, articulatory agility and syntactic structure, which are not always impacted in parallel. In this study, our first objective was to improve the characterization of connected speech production in each variant of primary progressive aphasia, by quantifying speech output along a number of motor speech and linguistic dimensions simultaneously. Secondly, we aimed to determine the neuroanatomical correlates of changes along these different dimensions. We recorded, transcribed and analysed speech samples for 50 patients with primary progressive aphasia, along with neurodegenerative and normal control groups. Patients were scanned with magnetic resonance imaging, and voxel-based morphometry was used to identify regions where atrophy correlated significantly with motor speech and linguistic features. Speech samples in patients with the non-fluent variant were characterized by slow rate, distortions, syntactic errors and reduced complexity. In contrast, patients with the semantic variant exhibited normal rate and very few speech or syntactic errors, but showed increased proportions of closed class words, pronouns and verbs, and higher frequency nouns, reflecting lexical retrieval deficits. In patients with the logopenic variant, speech rate (a common proxy for fluency) was intermediate between the other two variants, but distortions and syntactic errors were less common than in the non-fluent variant, while lexical access was less impaired than in the semantic variant. Reduced speech rate was linked with atrophy to a wide range of both anterior and posterior language regions, but specific deficits had more circumscribed anatomical correlates. Frontal regions were associated with motor speech and syntactic processes, anterior and inferior temporal regions with lexical retrieval, and posterior temporal regions with phonological errors and several other types of disruptions to fluency. These findings demonstrate that a multidimensional quantification of connected speech production is necessary to characterize the differences between the speech patterns of each primary progressive aphasic variant adequately, and to reveal associations between particular aspects of connected speech and specific components of the neural network for speech production.

Figure 1

Patient groups and stimulus material. (A) Regions of significant atrophy in each of the three PPA groups. These maps were derived by comparing each PPA patient group to 58 normal controls using voxelwise two-sample t-tests with independent variance, thresholded at voxelwise P < 10^–5, with a minimum cluster size of 1000 mm³. NFV = non-fluent variant; SV = semantic variant; LV = logopenic variant. (B) The picnic scene from the Western Aphasia Battery (Kertesz, 1982), which patients were asked to describe. Copyright © 2006 NCS Pearson Inc. Reproduced with permission. All rights reserved.

Figure 2

Speech rate and speech sound errors. (A) Overall speech rate in each of the five groups. Error bars show standard deviation. Each patient is represented by a circle, with outliers (>2 SD from the mean for the patient’s group) shaded grey. Within each patient group, patients are arranged from left to right in order of decreasing mini-mental state examination score, an approximate measure of disease progression. (B) Maximum speech rate. (C) Distortions. (D) Phonological paraphasias. (E) Voxel-based morphometry showing brain regions where atrophy was correlated with reduced maximum rate (red), increased numbers of distortions (blue) and increased numbers of phonological paraphasias (green). Statistical t maps were projected onto the lateral surface of the left hemisphere; also shown is a sagittal cut through the superior longitudinal fasciculus. Regions shown were statistically significant at P < 0.05 corrected for multiple comparisons based on cluster size, with the exception of the region associated with phonological paraphasias (dagger), which was only marginally significant (cluster size = 518 mm³, P = 0.012). wpm = words per minute; phw = per hundred words; NFV = non-fluent variant; SV = semantic variant; LV = logopenic variant; NC = normal controls.

Figure 3

Correlations between speech rate and two kinds of speech sound errors. (A) Correlations between maximum rate and distortions in each of the five patient groups. These variables were marginally correlated in non-fluent variant, as denoted by the fitted line. (B) Correlations between maximum rate and phonological paraphasias (none significant). (C) Correlations between distortions and phonological paraphasias (none significant). wpm = words per minute; phw = per hundred words; PC = principal component; Phon. = phonological; NFV = non-fluent variant; SV = semantic variant; LV = logopenic variant; NC = normal controls.

Figure 4

Other disruptions to fluency. (A) False starts. (B) Filled pauses. (C) Repaired sequences. (D) Incomplete sentences. (E) Voxel-based morphometry showing brain regions where atrophy was correlated with increased numbers of false starts (red), increased numbers of filled pauses (blue) and increased numbers of repaired sequences (green). phw = per hundred words; NFV = non-fluent variant; SV = semantic variant; LV = logopenic variant; NC = normal controls.

Figure 5

Lexical content. (A) Closed class words (as a proportion of all words). (B) Pronouns (as a proportion of all nominals, i.e. pronouns and nouns). (C) Verbs (as a proportion of the two major open classes, i.e. verbs and nouns). (D) Mean log frequency of nouns. (E) Voxel-based morphometry showing brain regions where atrophy was correlated with greater proportions of pronouns (red), greater proportions of verbs (blue) and higher frequency nouns (green). NFV = non-fluent variant; SV = semantic variant; LV = logopenic variant; NC = normal controls.

Figure 6

Syntactic structure and complexity. (A) Mean length of utterances. (B) Words in sentences (as a proportion of all words). (C) Syntactic errors. (D) A summary syntax measure, comprising the first principal component derived from words in sentences and syntactic errors. (E) Embeddings. (F) Semantic errors, i.e. sentences that were syntactically correct but semantically anomalous or inappropriate. (G) Voxel-based morphometry showing brain regions where atrophy was correlated with lower scores on the composite syntactic measure indicating greater syntactic impairments (red) and reduced numbers of embeddings (blue). The syntax measures were not used independently for voxel-based morphometry because they each captured only a subset of patients with syntactic deficits. Phw = per hundred words; NFV = non-fluent variant; SV = semantic variant; LV = logopenic variant; NC = normal controls; PC = principal component.

Figure 7

Correlations between syntactic measures and other measures. (A) The relationship between words in sentences and syntactic errors, showing how some patients with the non-fluent variant of PPA make many errors, whereas others often fail to produce complete sentences. (B) Correlations between repaired sequences and the composite syntactic measure. Only in the logopenic variant group, there was a significant association between these variables (fitted line). (C) Correlations between distortions and the composite syntactic measure, showing that patients with the non-fluent variant could be impaired on one or both of these measures. phw = per hundred words; NFV = non-fluent variant; SV = semantic variant; LV = logopenic variant; NC = normal controls.