Dataset Information

Network dysfunction predicts speech production after left hemisphere stroke.

ABSTRACT:

Objective

To investigate the role of multiple distributed brain networks, including the default mode, fronto-temporo-parietal, and cingulo-opercular networks, which mediate domain-general and task-specific processes during speech production after aphasic stroke.

Methods

We conducted an observational functional MRI study to investigate the effects of a previous left hemisphere stroke on functional connectivity within and between distributed networks as patients described pictures. Study design included various baseline tasks, and we compared results to those of age-matched healthy participants performing the same tasks. We used independent component and psychophysiological interaction analyses.

Results

Although activity within individual networks was not predictive of speech production, relative activity between networks was a predictor of both within-scanner and out-of-scanner language performance, over and above that predicted from lesion volume, age, sex, and years of education. Specifically, robust functional imaging predictors were the differential activity between the default mode network and both the left and right fronto-temporo-parietal networks, respectively activated and deactivated during speech. We also observed altered between-network functional connectivity of these networks in patients during speech production.

Conclusions

Speech production is dependent on complex interactions among widely distributed brain networks, indicating that residual speech production after stroke depends on more than the restoration of local domain-specific functions. Our understanding of the recovery of function following focal lesions is not adequately captured by consideration of ipsilesional or contralesional brain regions taking over lost domain-specific functions, but is perhaps best considered as the interaction between what remains of domain-specific networks and domain-general systems that regulate behavior.

SUBMITTER: Geranmayeh F

PROVIDER: S-EPMC4826341 | biostudies-literature | 2016 Apr

REPOSITORIES: biostudies-literature

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Publications

Network dysfunction predicts speech production after left hemisphere stroke.

Geranmayeh Fatemeh F Leech Robert R Wise Richard J S RJS

Neurology 20160309 14

<h4>Objective</h4>To investigate the role of multiple distributed brain networks, including the default mode, fronto-temporo-parietal, and cingulo-opercular networks, which mediate domain-general and task-specific processes during speech production after aphasic stroke.<h4>Methods</h4>We conducted an observational functional MRI study to investigate the effects of a previous left hemisphere stroke on functional connectivity within and between distributed networks as patients described pictures. ...[more]

PMID: 26962070

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Project description:Increasing evidence indicates that focal lesions following stroke cause alterations in connectivity among functional brain networks. Functional connectivity between hemispheres has been shown to be particularly critical for predicting stroke-related behavioral deficits and recovery of motor function and attention. Much less is known, however, about the relevance of interhemispheric functional connectivity for cognitive abilities like praxis that rely on strongly lateralized brain networks. In the current study, we examine correlations between symptoms of apraxia-a disorder of skilled action that cannot be attributed to lower-level sensory or motor impairments-and spontaneous, resting brain activity in functional MRI in chronic left hemisphere stroke patients and neurologically-intact control participants. Using a data-driven approach, we identified 32 regions-of-interest in which pairwise functional connectivity correlated with two distinct measures of apraxia, even when controlling for age, head motion, lesion volume, and other artifacts: overall ability to pantomime the typical use of a tool, and disproportionate difficulty pantomiming the use of tools associated with different, competing use and grasp-to-move actions (e.g., setting a kitchen timer versus picking it up). Better performance on both measures correlated with stronger interhemispheric functional connectivity. Relevant regions in the right hemisphere were often homologous to left hemisphere areas associated with tool use and action. Additionally, relative to overall pantomime accuracy, disproportionate difficulty pantomiming the use of tools associated with competing use and grasp actions was associated with weakened functional connectivity among a more strongly left-lateralized and peri-Sylvian set of brain regions. Finally, patient performance on both measures of apraxia was best predicted by a model that incorporated information about lesion location and functional connectivity, and functional connectivity continued to explain unique variance in behavior even after accounting for lesion loci. These results indicate that interhemispheric functional connectivity is relevant even for a strongly lateralized cognitive ability like praxis and emphasize the importance of the right hemisphere in skilled action.

Project description:Acquired language disorders after stroke are strongly associated with left hemisphere damage. When language difficulties are observed in the context of right hemisphere strokes, patients are usually considered to have atypical functional anatomy. By systematically integrating behavioural and lesion data from brain damaged patients with functional MRI data from neurologically normal participants, we investigated when and why right hemisphere strokes cause language disorders. Experiment 1 studied right-handed patients with unilateral strokes that damaged the right (n = 109) or left (n = 369) hemispheres. The most frequently impaired language task was: auditory sentence-to-picture matching after right hemisphere strokes; and spoken picture description after left hemisphere strokes. For those with auditory sentence-to-picture matching impairments after right hemisphere strokes, the majority (n = 9) had normal performance on tests of perceptual (visual or auditory) and linguistic (semantic, phonological or syntactic) processing. Experiment 2 found that these nine patients had significantly more damage to dorsal parts of the superior longitudinal fasciculus and the right inferior frontal sulcus compared to 75 other patients who also had right hemisphere strokes but were not impaired on the auditory sentence-to-picture matching task. Damage to these right hemisphere regions caused long-term speech comprehension difficulties in 67% of patients. Experiments 3 and 4 used functional MRI in two groups of 25 neurologically normal individuals to show that within the regions identified by Experiment 2, the right inferior frontal sulcus was normally activated by (i) auditory sentence-to-picture matching; and (ii) one-back matching when the demands on linguistic and non-linguistic working memory were high. Together, these experiments demonstrate that the right inferior frontal cortex contributes to linguistic and non-linguistic working memory capacity (executive function) that is needed for normal speech comprehension. Our results link previously unrelated literatures on the role of the right inferior frontal cortex in executive processing and the role of executive processing in sentence comprehension; which in turn helps to explain why right inferior frontal activity has previously been reported to increase during recovery of language function after left hemisphere stroke. The clinical relevance of our findings is that the detrimental effect of right hemisphere strokes on language is (i) much greater than expected; (ii) frequently observed after damage to the right inferior frontal sulcus; (iii) task dependent; (iv) different to the type of impairments observed after left hemisphere strokes; and (v) can result in long-lasting deficits that are (vi) not the consequence of atypical language lateralization.

Project description:The neural mechanisms underlying recovery of language after left hemisphere stroke remain elusive. Although older evidence suggested that right hemisphere language homologues compensate for damage in left hemisphere language areas, the current prevailing theory suggests that right hemisphere engagement is ineffective or even maladaptive. Using a novel combination of support vector regression-based lesion-symptom mapping and voxel-based morphometry, we aimed to determine whether local grey matter volume in the right hemisphere independently contributes to aphasia outcomes after chronic left hemisphere stroke. Thirty-two left hemisphere stroke survivors with aphasia underwent language assessment with the Western Aphasia Battery-Revised and tests of other cognitive domains. High-resolution T1-weighted images were obtained in aphasia patients and 30 demographically matched healthy controls. Support vector regression-based multivariate lesion-symptom mapping was used to identify critical language areas in the left hemisphere and then to quantify each stroke survivor's lesion burden in these areas. After controlling for these direct effects of the stroke on language, voxel-based morphometry was then used to determine whether local grey matter volumes in the right hemisphere explained additional variance in language outcomes. In brain areas in which grey matter volumes related to language outcomes, we then compared grey matter volumes in patients and healthy controls to assess post-stroke plasticity. Lesion-symptom mapping showed that specific left hemisphere regions related to different language abilities. After controlling for lesion burden in these areas, lesion size, and demographic factors, grey matter volumes in parts of the right temporoparietal cortex positively related to spontaneous speech, naming, and repetition scores. Examining whether domain general cognitive functions might explain these relationships, partial correlations demonstrated that grey matter volumes in these clusters related to verbal working memory capacity, but not other cognitive functions. Further, grey matter volumes in these areas were greater in stroke survivors than healthy control subjects. To confirm this result, 10 chronic left hemisphere stroke survivors with no history of aphasia were identified. Grey matter volumes in right temporoparietal clusters were greater in stroke survivors with aphasia compared to those without history of aphasia. These findings suggest that the grey matter structure of right hemisphere posterior dorsal stream language homologues independently contributes to language production abilities in chronic left hemisphere stroke, and that these areas may undergo hypertrophy after a stroke causing aphasia.

Project description:When pantomiming the use of tools, patients with limb apraxia after left hemisphere stroke (LCVA) produce more spatiotemporal hand action errors with tools associated with conflicting actions for use versus grasp-to-pick-up (e.g., corkscrew) than tools having a single action for both use and grasp (e.g., hammer). There are two possible accounts for this pattern of results. Reduced performance with 'conflict' tools may simply reflect weakened automaticity of use action activation, which is evident only when the use and grasp actions are not redundant. Alternatively, poor use performance may reflect a reduced ability of appropriate tool use actions to compete with task-inappropriate action representations. To address this issue, we developed a Stroop-like experiment in which 21 LCVA and 8 neurotypical participants performed pantomime actions in blocks containing two tools that were similar ("neighbors") in terms of hand action or function, or were unrelated on either dimension. In a congruent condition, they pantomimed the use action associated with the visually presented tool, whereas in an incongruent condition, they pantomimed the use action for the other tool in the block. Relative to controls and other task conditions, LCVA participants showed reductions in hand action errors in incongruent relative to congruent action trials; furthermore, the degree of reduction in this incongruence effect was related to the participants' susceptibility to grasp-on-use conflict in a separate test of pantomime to the sight of tools. Support vector regression lesion-symptom mapping analyses identified the left inferior frontal gyrus, supramarginal gyrus, and superior longitudinal fasciculus as core neuroanatomical sites associated with abnormal performance. Collectively, the results indicate that weakened activation of tool use actions in limb apraxia gives rise to reduced ability of these actions to compete for task-appropriate selection when competition arises within single tools (grasp-on-use conflict) as well as between two tools (reduced neighborhood effects).

Project description:Depending on the lesion site, a stroke typically affects various aspects of cognitive control. While executing a task, the performance monitoring system constantly compares an intended action plan with the executed action and thereby registers inaccurate actions in case of any mismatch. When errors occur, the performance monitoring system signals the need for more cognitive control, which is most efficient when the subject notices errors rather than processing them subconsciously. The current study aimed to investigate performance monitoring and error detection in a large sample of patients with left hemisphere (LH) stroke. In addition to clinical and neuropsychological tests, 24 LH stroke patients and 32 healthy age-matched controls performed a Go/Nogo task with simultaneous electroencephalography (EEG) measurements. This set-up enabled us to compare performance monitoring at the behavioral and the neural level. EEG data were analyzed using event-related potentials [ERPs; e.g., the error-related negativity (Ne/ERN) and error positivity (Pe)] and additionally more sensitive whole-brain multivariate pattern classification analyses (MVPA). We hypothesized that LH stroke patients would show behavioural deficits in error detection when compared to healthy controls, mirrored by differences in neural signals, in particular reflected in the Pe component. Interestingly, despite clinically relevant cognitive deficits (e.g., aphasia and apraxia) including executive dysfunction (trail making test), we did not observe any behavioral impairments related to performance monitoring and error processing in the current LH stroke patients. Patients also showed similar results for Ne/ERN and Pe components, compared to the control group, and a highly similar prediction of errors from multivariate signals. ERP abnormalities during stimulus processing (i.e., N2 and P3) demonstrated the specificity of these findings in the current LH stroke patients. In contrast to previous studies, by employing a relatively large patient sample, a well-controlled experimental paradigm with a standardized error signaling procedure, and advanced data analysis, we were able to show that performance monitoring (of simple actions) is a preserved cognitive control function in LH stroke patients that might constitute a useful resource in rehabilitative therapies for re-learning impeded functions.

Dataset Information

Network dysfunction predicts speech production after left hemisphere stroke.

Objective

Methods

Results

Conclusions

Publications

Network dysfunction predicts speech production after left hemisphere stroke.

Similar Datasets

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