Four dimensions of naturalistic language production in aphasia after stroke.

There is a rich tradition of research on the neuroanatomical correlates of spoken language production in aphasia using constrained tasks (e.g., picture naming), which offer controlled insights into the distinct processes that govern speech and language (i.e., lexical-semantic access, morphosyntactic construction, phonological encoding, speech motor programming/execution). Yet these tasks do not necessarily reflect everyday language use. In contrast, naturalistic language production (also referred to as connected speech or discourse) more closely approximates typical processing demands, requiring the dynamic integration of all aspects of speech and language. The brain bases of naturalistic language production remain relatively unknown, however, in part because of the difficulty in deriving features that are salient, quantifiable, and interpretable relative to both speech-language processes and the extant literature. The present cross-sectional observational study seeks to address these challenges by leveraging a validated and comprehensive auditory-perceptual measurement system that yields four explanatory dimensions of performance-Paraphasia (misselection of words and sounds), Logopenia (paucity of words), Agrammatism (grammatical omissions), and Motor speech (impaired speech motor programming/execution). We used this system to characterize naturalistic language production in a large and representative sample of individuals with acute post-stroke aphasia (n = 118). Scores on each of the four dimensions were correlated with lesion metrics, and multivariate associations among the dimensions and brain regions were then explored. Our findings revealed distinct yet overlapping neuroanatomical correlates throughout the left-hemisphere language network. Paraphasia and Logopenia were associated primarily with posterior regions, spanning both dorsal and ventral streams, which are critical for lexical-semantic access and phonological encoding. In contrast, Agrammatism and Motor speech were associated primarily with anterior regions of the dorsal stream that are involved in morphosyntactic construction and speech motor planning/execution respectively. Collectively, we view these results as constituting a brain-behavior model of naturalistic language production in aphasia, aligning with both historical and contemporary accounts of the neurobiology of spoken language production.

Situating word deafness within aphasia recovery: A case report.

Word deafness is a rare neurological disorder often observed following bilateral damage to superior temporal cortex and canonically defined as an auditory modality-specific deficit in word comprehension. The extent to which word deafness is dissociable from aphasia remains unclear given its heterogeneous presentation, and some have consequently posited that word deafness instead represents a stage in recovery from aphasia, where auditory and linguistic processing are affected to varying degrees and improve at differing rates. Here, we report a case of an individual (Mr. C) with bilateral temporal lobe lesions whose presentation evolved from a severe aphasia to an atypical form of word deafness, where auditory linguistic processing was impaired at the sentence level and beyond. We first reconstructed in detail Mr. C's stroke recovery through medical record review and supplemental interviewing. Then, using behavioral testing and multimodal neuroimaging, we documented a predominant auditory linguistic deficit in sentence and narrative comprehension-with markedly reduced behavioral performance and absent brain activation in the language network in the spoken modality exclusively. In contrast, Mr. C displayed near-unimpaired behavioral performance and robust brain activations in the language network for the linguistic processing of words, irrespective of modality. We argue that these findings not only support the view of word deafness as a stage in aphasia recovery but also further instantiate the important role of left superior temporal cortex in auditory linguistic processing.

Multivariate lesion symptom mapping for predicting trajectories of recovery from aphasia.

Individuals with post-stroke aphasia tend to recover their language to some extent; however, it remains challenging to reliably predict the nature and extent of recovery that will occur in the long term. The aim of this study was to quantitatively predict language outcomes in the first year of recovery from aphasia across multiple domains of language and at multiple timepoints post-stroke. We recruited 217 patients with aphasia following acute left hemisphere ischaemic or haemorrhagic stroke and evaluated their speech and language function using the Quick Aphasia Battery acutely and then acquired longitudinal follow-up data at up to three timepoints post-stroke: 1 month (n = 102), 3 months (n = 98) and 1 year (n = 74). We used support vector regression to predict language outcomes at each timepoint using acute clinical imaging data, demographic variables and initial aphasia severity as input. We found that ∼60% of the variance in long-term (1 year) aphasia severity could be predicted using these models, with detailed information about lesion location importantly contributing to these predictions. Predictions at the 1- and 3-month timepoints were somewhat less accurate based on lesion location alone, but reached comparable accuracy to predictions at the 1-year timepoint when initial aphasia severity was included in the models. Specific subdomains of language besides overall severity were predicted with varying but often similar degrees of accuracy. Our findings demonstrate the feasibility of using support vector regression models with leave-one-out cross-validation to make personalized predictions about long-term recovery from aphasia and provide a valuable neuroanatomical baseline upon which to build future models incorporating information beyond neuroanatomical and demographic predictors.

Leukoaraiosis Is Not Associated With Recovery From Aphasia in the First Year After Stroke.

After a stroke, individuals with aphasia often recover to a certain extent over time. This recovery process may be dependent on the health of surviving brain regions. Leukoaraiosis (white matter hyperintensities on MRI reflecting cerebral small vessel disease) is one indication of compromised brain health and is associated with cognitive and motor impairment. Previous studies have suggested that leukoaraiosis may be a clinically relevant predictor of aphasia outcomes and recovery, although findings have been inconsistent. We investigated the relationship between leukoaraiosis and aphasia in the first year after stroke. We recruited 267 patients with acute left hemispheric stroke and coincident fluid attenuated inversion recovery MRI. Patients were evaluated for aphasia within 5 days of stroke, and 174 patients presented with aphasia acutely. Of these, 84 patients were evaluated at ∼3 months post-stroke or later to assess longer-term speech and language outcomes. Multivariable regression models were fit to the data to identify any relationships between leukoaraiosis and initial aphasia severity, extent of recovery, or longer-term aphasia severity. We found that leukoaraiosis was present to varying degrees in 90% of patients. However, leukoaraiosis did not predict initial aphasia severity, aphasia recovery, or longer-term aphasia severity. The lack of any relationship between leukoaraiosis severity and aphasia recovery may reflect the anatomical distribution of cerebral small vessel disease, which is largely medial to the white matter pathways that are critical for speech and language function.

Modality-Specificity of the Neural Correlates of Linguistic and Non-Linguistic Demand.

Imaging studies of language processing in clinical populations can be complicated to interpret for several reasons, one being the difficulty of matching the effortfulness of processing across individuals or tasks. To better understand how effortful linguistic processing is reflected in functional activity, we investigated the neural correlates of task difficulty in linguistic and non-linguistic contexts in the auditory modality and then compared our findings to a recent analogous experiment in the visual modality in a different cohort. Nineteen neurologically normal individuals were scanned with fMRI as they performed a linguistic task (semantic matching) and a non-linguistic task (melodic matching), each with two levels of difficulty. We found that left hemisphere frontal and temporal language regions, as well as the right inferior frontal gyrus, were modulated by linguistic demand and not by non-linguistic demand. This was broadly similar to what was previously observed in the visual modality. In contrast, the multiple demand (MD) network, a set of brain regions thought to support cognitive flexibility in many contexts, was modulated neither by linguistic demand nor by non-linguistic demand in the auditory modality. This finding was in striking contradistinction to what was previously observed in the visual modality, where the MD network was robustly modulated by both linguistic and non-linguistic demand. Our findings suggest that while the language network is modulated by linguistic demand irrespective of modality, modulation of the MD network by linguistic demand is not inherent to linguistic processing, but rather depends on specific task factors.

Recovery from aphasia in the first year after stroke.

Most individuals who experience aphasia after a stroke recover to some extent, with the majority of gains taking place in the first year. The nature and time course of this recovery process is only partially understood, especially its dependence on lesion location and extent, which are the most important determinants of outcome. The aim of this study was to provide a comprehensive description of patterns of recovery from aphasia in the first year after stroke. We recruited 334 patients with acute left hemisphere supratentorial ischaemic or haemorrhagic stroke and evaluated their speech and language function within 5 days using the Quick Aphasia Battery (QAB). At this initial time point, 218 patients presented with aphasia. Individuals with aphasia were followed longitudinally, with follow-up evaluations of speech and language at 1 month, 3 months, and 1 year post-stroke, wherever possible. Lesions were manually delineated based on acute clinical MRI or CT imaging. Patients with and without aphasia were divided into 13 groups of individuals with similar, commonly occurring patterns of brain damage. Trajectories of recovery were then investigated as a function of group (i.e. lesion location and extent) and speech/language domain (overall language function, word comprehension, sentence comprehension, word finding, grammatical construction, phonological encoding, speech motor programming, speech motor execution, and reading). We found that aphasia is dynamic, multidimensional, and gradated, with little explanatory role for aphasia subtypes or binary concepts such as fluency. Patients with circumscribed frontal lesions recovered well, consistent with some previous observations. More surprisingly, most patients with larger frontal lesions extending into the parietal or temporal lobes also recovered well, as did patients with relatively circumscribed temporal, temporoparietal, or parietal lesions. Persistent moderate or severe deficits were common only in patients with extensive damage throughout the middle cerebral artery distribution or extensive temporoparietal damage. There were striking differences between speech/language domains in their rates of recovery and relationships to overall language function, suggesting that specific domains differ in the extent to which they are redundantly represented throughout the language network, as opposed to depending on specialized cortical substrates. Our findings have an immediate clinical application in that they will enable clinicians to estimate the likely course of recovery for individual patients, as well as the uncertainty of these predictions, based on acutely observable neurological factors.

An open dataset of connected speech in aphasia with consensus ratings of auditory-perceptual features.

Purpose: Auditory-perceptual rating of connected speech in aphasia (APROCSA) involves trained listeners rating a large number of perceptual features of speech samples, and has shown promise as an approach for quantifying expressive speech and language function in individuals with aphasia. The aim of this study was to obtain consensus ratings for a diverse set of speech samples, which can then be used as training materials for learning the APROCSA system. Method: Connected speech samples were recorded from six individuals with chronic post-stroke aphasia. A segment containing the first five minutes of participant speech was excerpted from each sample, and 27 features were rated on a five-point scale by five researchers. The researchers then discussed each feature in turn to obtain consensus ratings. Results: Six connected speech samples are made freely available for research, education, and clinical uses. Consensus ratings are reported for each of the 27 features, for each speech sample. Discrepancies between raters were resolved through discussion, yielding consensus ratings that can be expected to be more accurate than mean ratings. Conclusions: The dataset will provide a useful resource for scientists, students, and clinicians to learn how to evaluate aphasic speech samples with an auditory-perceptual approach.

Neuroplasticity in post-stroke aphasia: A systematic review and meta-analysis of functional imaging studies of reorganization of language processing.

Recovery from aphasia is thought to depend on neural plasticity, that is, functional reorganization of surviving brain regions such that they take on new or expanded roles in language processing. We carried out a systematic review and meta-analysis of all articles published between 1995 and early 2020 that have described functional imaging studies of six or more individuals with post-stroke aphasia, and have reported analyses bearing on neuroplasticity of language processing. Each study was characterized and appraised in detail, with particular attention to three critically important methodological issues: task performance confounds, contrast validity, and correction for multiple comparisons. We identified 86 studies describing a total of 561 relevant analyses. We found that methodological limitations related to task performance confounds, contrast validity, and correction for multiple comparisons have been pervasive. Only a few claims about language processing in individuals with aphasia are strongly supported by the extant literature: first, left hemisphere language regions are less activated in individuals with aphasia than neurologically normal controls, and second, in cohorts with aphasia, activity in left hemisphere language regions, and possibly a temporal lobe region in the right hemisphere, is positively correlated with language function. There is modest, equivocal evidence for the claim that individuals with aphasia differentially recruit right hemisphere homotopic regions, but no compelling evidence for differential recruitment of additional left hemisphere regions or domain-general networks. There is modest evidence that left hemisphere language regions return to function over time, but no compelling longitudinal evidence for dynamic reorganization of the language network.

Unexpected absence of aphasia following left temporal hemorrhage: a case study with functional neuroimaging to characterize the nature of atypical language localization.

Unexpected absence of aphasia after left-hemisphere perisylvian damage is often assumed to reflect right-hemisphere language lateralization, but other potential explanations include bilateral language representation, or sparing of critical left-hemisphere regions due to individual variability. We describe the case of a left-handed gentleman who presented with no aphasia after a left temporal hemorrhage. We used functional neuroimaging to determine how his language network had been spared. In this case, we observed unequivocal right-hemisphere lateralization of language function, explaining his lack of aphasia. We discuss the variability of language organization and highlight outstanding questions about the implications of damage in different scenarios.

Language Mapping in Aphasia.

Purpose Recovery from aphasia is thought to depend on neural plasticity, that is, functional reorganization of surviving brain regions such that they take on new or expanded roles in language processing. To make progress in characterizing the nature of this process, we need feasible, reliable, and valid methods for identifying language regions of the brain in individuals with aphasia. This article reviews 3 recent studies from our lab in which we have developed and validated several novel functional magnetic resonance imaging paradigms for language mapping in aphasia. Method In the 1st study, we investigated the reliability and validity of 4 language mapping paradigms in neurologically normal older adults. In the 2nd study, we developed a novel adaptive semantic matching paradigm and assessed its feasibility, reliability, and validity in individuals with and without aphasia. In the 3rd study, we developed and evaluated 2 additional adaptive paradigms-rhyme judgment and syllable counting-for mapping phonological encoding regions. Results We found that the adaptive semantic matching paradigm could be performed by most individuals with aphasia and yielded reliable and valid maps of core perisylvian language regions in each individual participant. The psychometric properties of this paradigm were superior to those of other commonly used paradigms such as narrative comprehension and picture naming. The adaptive rhyme judgment paradigm was capable of identifying fronto-parietal phonological encoding regions in individual participants. Conclusion Adaptive language mapping paradigms offer a promising approach for future research on the neural basis of recovery from aphasia. Presentation Video https://doi.org/10.23641/asha.10257584.

Patterns of Recovery From Aphasia in the First 2 Weeks After Stroke.

Purpose Recovery from aphasia after stroke has a decelerating trajectory, with the greatest gains taking place early and the slope of change decreasing over time. Despite its importance, little is known regarding evolution of language function in the early postonset period. The goal of this study was to characterize the dynamics and nature of recovery of language function in the acute and early subacute phases of stroke. Method Twenty-one patients with aphasia were evaluated every 2-3 days for the first 15 days after onset of acute ischemic or hemorrhagic stroke. Language function was assessed at each time point with the Quick Aphasia Battery (Wilson, Eriksson, Schneck, & Lucanie, 2018), which yields an overall summary score and a multidimensional profile of 7 different language domains. Results On a 10-point scale, overall language function improved by a mean of 1.07 points per week, confidence interval [0.46, 1.71], with 19 of 21 patients showing positive changes. The trajectory of recovery was approximately linear over this time period. There was significant variability across patients, and patients with more impaired language function at Day 2 poststroke experienced greater improvements over the subsequent 2 weeks. Patterns of recovery differed across language domains, with consistent improvements in word finding, grammatical construction, repetition, and reading, but less consistent improvements in word comprehension and sentence comprehension. Conclusion Overall language function typically improves substantially and steadily during the first 2 weeks after stroke, driven mostly by recovery of expressive language. Information on the trajectory of early recovery will increase the accuracy of prognoses and establish baseline expectations against which to evaluate the efficacy of interventions. Supplemental Material https://doi.org/10.23641/asha.7811876.

Correction: A quick aphasia battery for efficient, reliable, and multidimensional assessment of language function.

[This corrects the article DOI: 10.1371/journal.pone.0192773.].

A quick aphasia battery for efficient, reliable, and multidimensional assessment of language function.

This paper describes a quick aphasia battery (QAB) that aims to provide a reliable and multidimensional assessment of language function in about a quarter of an hour, bridging the gap between comprehensive batteries that are time-consuming to administer, and rapid screening instruments that provide limited detail regarding individual profiles of deficits. The QAB is made up of eight subtests, each comprising sets of items that probe different language domains, vary in difficulty, and are scored with a graded system to maximize the informativeness of each item. From the eight subtests, eight summary measures are derived, which constitute a multidimensional profile of language function, quantifying strengths and weaknesses across core language domains. The QAB was administered to 28 individuals with acute stroke and aphasia, 25 individuals with acute stroke but no aphasia, 16 individuals with chronic post-stroke aphasia, and 14 healthy controls. The patients with chronic post-stroke aphasia were tested 3 times each and scored independently by 2 raters to establish test-retest and inter-rater reliability. The Western Aphasia Battery (WAB) was also administered to these patients to assess concurrent validity. We found that all QAB summary measures were sensitive to aphasic deficits in the two groups with aphasia. All measures showed good or excellent test-retest reliability (overall summary measure: intraclass correlation coefficient (ICC) = 0.98), and excellent inter-rater reliability (overall summary measure: ICC = 0.99). Sensitivity and specificity for diagnosis of aphasia (relative to clinical impression) were 0.91 and 0.95 respectively. All QAB measures were highly correlated with corresponding WAB measures where available. Individual patients showed distinct profiles of spared and impaired function across different language domains. In sum, the QAB efficiently and reliably characterized individual profiles of language deficits.