Neuroimaging correlates of language network impairment and reorganization in temporal lobe epilepsy

Balter, Susan G. T.; Lin, Grace C.; Leyden, Kelly M.; Paul, Brianna M.; McDonald, Carrie R.

doi:10.1016/j.bandl.2016.06.002

Cited by 35 publications

(24 citation statements)

References 143 publications

(189 reference statements)

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“…2A and Supporting Information, Table S1). Evidence of abnormal language networks in TLE has been consistently described and interpreted in association with language deficits (see reviews by Balter et al, 2016 andHamberger andCole, 2011). These areas have been associated with various aspects of reading and lexical responses (Schwartz et al, 1999).…”

Section: Discussionmentioning

confidence: 99%

From “rest” to language task: Task activation selects and prunes from broader resting‐state network

Doucet

Sperling

et al. 2017

Human Brain Mapping

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Resting-state networks (RSNs) show spatial patterns generally consistent with networks revealed during cognitive tasks. However, the exact degree of overlap between these networks has not been clearly quantified. Such an investigation shows promise for decoding altered functional connectivity (FC) related to abnormal language functioning in clinical populations such as temporal lobe epilepsy (TLE). In this context, we investigated the network configurations during a language task and during resting state using FC. Twenty-four healthy controls, 24 right and 24 left TLE patients completed a verb generation (VG) task and a resting-state fMRI scan. We compared the language network revealed by the VG task with three FC-based networks (seeding the left inferior frontal cortex (IFC)/Broca): two from the task (ON, OFF blocks) and one from the resting state. We found that, for both left TLE patients and controls, the RSN recruited regions bilaterally, whereas both VG-on and VG-off conditions produced more left-lateralized FC networks, matching more closely with the activated language network. TLE brings with it variability in both task-dependent and task-independent networks, reflective of atypical language organization. Overall, our findings suggest that our RSN captured bilateral activity, reflecting a set of prepotent language regions. We propose that this relationship can be best understood by the notion of pruning or winnowing down of the larger language-ready RSN to carry out specific task demands. Our data suggest that multiple types of network analyses may be needed to decode the association between language deficits and the underlying functional mechanisms altered by disease. Hum Brain Mapp 38:2540-2552, 2017. © 2017 Wiley Periodicals, Inc.

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Section: Discussionmentioning

confidence: 99%

From “rest” to language task: Task activation selects and prunes from broader resting‐state network

Doucet

Sperling

et al. 2017

Human Brain Mapping

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“…Interestingly, our lexical‐semantic task was associated with preserved left frontal activation in TLE‐LI. This is important to note, because many fMRI tasks currently implemented for language mapping (eg, covert word generation) primarily demonstrate robust and reliable frontal lobe activations but less reliable temporal lobe activations. Our findings suggest that lexical‐semantic tasks designed to elicit temporal lobe activation may be a promising way to assess language network dysfunction in TLE.…”

Section: Discussionmentioning

confidence: 99%

“…For use in the ROI analysis, fMRI voxel activations were corrected for multiple comparisons by using a significance level of P < .01 and a cluster size ≥ 20, for a corrected α of .05 as determined by 3dClustSim. To probe possible network reorganization differences between groups, language laterality indices were calculated (LI = [L − R] / [L + R]) using a lateral temporal ROI …”

Section: Methodsmentioning

confidence: 99%

“…Language impairments are a widespread comorbidity in TLE. 6 Among our cognitive phenotypes, 49% of patients fell within a "language-impaired" group, characterized by deficits on neuropsychological tests of naming and fluency. 5 Although many studies report greater language impairment in patients with left TLE (LTLE) relative to right TLE (RTLE), [7][8][9] an emerging literature has highlighted that patients with RTLE also present with language impairment, [10][11][12] and sometimes LTLE and RTLE are indistinguishable in language performance.…”

Section: Introductionmentioning

confidence: 99%

“…Language impairments are a widespread comorbidity in TLE . Among our cognitive phenotypes, 49% of patients fell within a “language‐impaired” group, characterized by deficits on neuropsychological tests of naming and fluency .…”

Section: Introductionmentioning

confidence: 99%

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Identifying the neural basis of a language‐impaired phenotype of temporal lobe epilepsy

et al. 2019

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Objective To identify neuroimaging and clinical biomarkers associated with a language‐impaired phenotype in refractory temporal lobe epilepsy (TLE). Methods Eighty‐five patients with TLE were characterized as language‐impaired (TLE‐LI) or non–language‐impaired (TLE‐NLI) based on comprehensive neuropsychological testing. Structural magnetic resonance imaging (MRI), diffusion tensor imaging, and functional MRI (fMRI) were obtained in patients and 47 healthy controls (HC). fMRI activations and cortical thickness were calculated within language regions of interest, and fractional anisotropy (FA) was calculated within deep white matter tracts associated with language. Analyses of variance were performed to test for differences among the groups in imaging measures. Receiver operator characteristic curves were used to determine how well different clinical versus imaging measures discriminated TLE‐LI from TLE‐NLI. Results TLE‐LI patients showed significantly less activation within left superior temporal cortex compared to HC and TLE‐NLI, regardless of side of seizure onset. TLE‐LI also showed decreased FA in the inferior longitudinal fasciculus and arcuate fasciculus compared to HC. Cortical thickness did not differ between groups in any region. A model that included language‐related fMRI activations within the superior temporal gyrus, age at onset, and demographic variables was the most predictive of language impairment (area under the curve = 0.80). Significance These findings demonstrate a unique imaging signature associated with a language‐impaired phenotype in TLE, characterized by functional and microstructural alterations within the language network. Reduced left superior temporal activation combined with compromise to language association tracts underlies this phenotype, extending our previous work on cognitive phenotypes that could have implications for treatment‐planning or cognitive progression in TLE.

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More widespread functionality of posterior language area in patients with brain tumors

Nakajima,

Osada,

Kinoshita

et al. 2024

Human Brain Mapping

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Damage to the posterior language area (PLA), or Wernicke's area causes cortical reorganization in the corresponding regions of the contralateral hemisphere. However, the details of reorganization within the ipsilateral hemisphere are not fully understood. In this context, direct electrical stimulation during awake surgery can provide valuable opportunities to investigate neuromodulation of the human brain in vivo, which is difficult through the non‐invasive approaches. Thus, in this study, we aimed to investigate the characteristics of the cortical reorganization of the PLA within the ipsilateral hemisphere. Sixty‐two patients with left hemispheric gliomas were divided into groups depending on whether the lesion extended to the PLA. All patients underwent direct cortical stimulation with a picture‐naming task. We further performed functional connectivity analyses using resting‐state functional magnetic resonance imaging (MRI) in a subset of patients and calculated betweenness centrality, an index of the network importance of brain areas. During direct cortical stimulation, the regions showing positive (impaired) responses in the non‐PLA group were localized mainly in the posterior superior temporal gyrus (pSTG), whereas those in the PLA group were widely distributed from the pSTG to the posterior supramarginal gyrus (pSMG). Notably, the percentage of positive responses in the pSMG was significantly higher in the PLA group (47%) than in the non‐PLA group (8%). In network analyses of functional connectivity, the pSMG was identified as a hub region with high betweenness centrality in both the groups. These findings suggest that the language area can spread beyond the PLA to the pSMG, a hub region, in patients with lesion progression to the pSTG. The change in the pattern of the language area may be a compensatory mechanism to maintain efficient brain networks.

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Neuroimaging correlates of language network impairment and reorganization in temporal lobe epilepsy

Cited by 35 publications

References 143 publications

From “rest” to language task: Task activation selects and prunes from broader resting‐state network

From “rest” to language task: Task activation selects and prunes from broader resting‐state network

Identifying the neural basis of a language‐impaired phenotype of temporal lobe epilepsy

More widespread functionality of posterior language area in patients with brain tumors

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