Dynamic degree centrality in stroke-induced Broca's aphasia varies based on first language: A functional MRI study.
Broca aphasia
dynamic degree centrality
resting‐state fMRI
Journal
Journal of neuroimaging : official journal of the American Society of Neuroimaging
ISSN: 1552-6569
Titre abrégé: J Neuroimaging
Pays: United States
ID NLM: 9102705
Informations de publication
Date de publication:
22 Aug 2024
22 Aug 2024
Historique:
revised:
02
08
2024
received:
11
04
2024
accepted:
10
08
2024
medline:
23
8
2024
pubmed:
23
8
2024
entrez:
23
8
2024
Statut:
aheadofprint
Résumé
This study sought to explore dynamic degree centrality (DC) variability in particular regions of the brain in patients with poststroke Broca aphasia (BA) using a resting-state functional magnetic resonance imaging (rs-fMRI) approach, comparing differences between Uyghur and Chinese BA patients. This study investigated two factors, language and BA status, and divided patients into four groups: Uyghur aphasia patients (UA), Uyghur normal control subjects (UN), Chinese aphasia patients (CA), and Chinese normal subjects (CN) who underwent rs-fMRI analysis. Two-way analysis of variance (ANOVA) was used to calculate the comprehensive differences in dynamic DC among these four groups. Correlations between DC and language behavior were assessed with partial correlation analyses. Two-way ANOVA revealed comparable results for the results of pairwise comparisons of dynamic DC variability among the four groups in the right middle frontal gyrus/orbital part (ORBmid.R), right superior frontal gyrus/dorsolateral, and right precuneus (PCUN.R), with results as follows: UA < UN, CA > CN, UA < CA, and UN > CN (p < .05, with the exception of the p-values for UA and UN in superior frontal gyrus/dorsolateral). In contrast, the opposite results were observed for the right calcarine fissure and surrounding cortex (CAL.R, p < .05). The observed enhancement of dynamic DC variability in ORBmid.R and PCUN.R among Chinese BA patients and in CAL.R in Uyghur BA patients may be attributable to language network restructuring. Overall, these results suggest that BA patients who use different language families may exhibit differences in the network mechanisms that characterize observed impairments of language function.
Sections du résumé
BACKGROUND AND PURPOSE
OBJECTIVE
This study sought to explore dynamic degree centrality (DC) variability in particular regions of the brain in patients with poststroke Broca aphasia (BA) using a resting-state functional magnetic resonance imaging (rs-fMRI) approach, comparing differences between Uyghur and Chinese BA patients.
METHODS
METHODS
This study investigated two factors, language and BA status, and divided patients into four groups: Uyghur aphasia patients (UA), Uyghur normal control subjects (UN), Chinese aphasia patients (CA), and Chinese normal subjects (CN) who underwent rs-fMRI analysis. Two-way analysis of variance (ANOVA) was used to calculate the comprehensive differences in dynamic DC among these four groups. Correlations between DC and language behavior were assessed with partial correlation analyses.
RESULTS
RESULTS
Two-way ANOVA revealed comparable results for the results of pairwise comparisons of dynamic DC variability among the four groups in the right middle frontal gyrus/orbital part (ORBmid.R), right superior frontal gyrus/dorsolateral, and right precuneus (PCUN.R), with results as follows: UA < UN, CA > CN, UA < CA, and UN > CN (p < .05, with the exception of the p-values for UA and UN in superior frontal gyrus/dorsolateral). In contrast, the opposite results were observed for the right calcarine fissure and surrounding cortex (CAL.R, p < .05).
CONCLUSION
CONCLUSIONS
The observed enhancement of dynamic DC variability in ORBmid.R and PCUN.R among Chinese BA patients and in CAL.R in Uyghur BA patients may be attributable to language network restructuring. Overall, these results suggest that BA patients who use different language families may exhibit differences in the network mechanisms that characterize observed impairments of language function.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Shanghai Pudong New Area Science and Technology development Fund
ID : PKJ2022-Y30
Organisme : TCM rehabilitation Plateau Discipline
ID : YC-2023-0606
Informations de copyright
© 2024 The Author(s). Journal of Neuroimaging published by Wiley Periodicals LLC on behalf of American Society of Neuroimaging.
Références
Klingbeil J, Wawrzyniak M, Stockert A, et al. Resting‐state functional connectivity: an emerging method for the study of language networks in post‐stroke aphasia. Brain Cogn. 2019;131:22–33.
Baldassarre A, Metcalf NV, Shulman GL, et al. Brain networks' functional connectivity separates aphasic deficits in stroke. Neurology. 2019;92:e125–e135.
Lazar RM, Boehme AK. Aphasia as a predictor of stroke outcome. Curr Neurol Neurosci Rep. 2017;17:1–5.
Gerstenecker A, Lazar RM. Language recovery following stroke. Clin Neuropsychol. 2019;33:928–947.
Friederici AD. The brain basis of language processing: from structure to function. Physiol Rev. 2011;91:1357–1392.
Broca P. Nouvelle observation d'aphémie produite par une lésion de la moitié postérieure des deuxième et troisième circonvolutions frontales. Bull Soc Chim Fr. 1861;36:398–407.
Dronkers NF, Plaisant O, Iba‐Zizen MT, et al. Paul Broca's historic cases: high resolution MR imaging of the brains of Leborgne and Lelong. Brain. 2007;130:1432–1441.
Radanovic M, Scaff M. Speech and language disturbances due to subcortical lesions. Brain Lang. 2003;84:337–352.
Gajardo‐Vidal A, Lorca‐Puls DL, Team P, et al. Damage to Broca's area does not contribute to long‐term speech production outcome after stroke. Brain. 2021;144:817–832.
Jackson RL. The neural correlates of semantic control revisited. Neuroimage. 2021;224:117444.
Turker S, Kuhnke P, Eickhoff SB, et al. Cortical, subcortical, and cerebellar contributions to language processing: a meta‐analytic review of 403 neuroimaging experiments. Psychol Bull. 2023;14911‐1:699–723. https://doi.org/10.1037/bul0000403
Cohen Z, Steinbrenner M, Piper RJ, et al. Transcranial electrical stimulation during functional magnetic resonance imaging in patients with genetic generalized epilepsy: a pilot and feasibility study. Front Neurosci. 2024;18:1354523.
Shan A, Zhang H, Gao M, et al. Aberrant voxel‐based degree centrality and functional connectivity in Parkinson's disease patients with fatigue. CNS Neurosci Ther. 2023;29:2680–2689.
Audrain S, Barnett AJ, McAndrews MP. Language network measures at rest indicate individual differences in naming decline after anterior temporal lobe resection. Hum Brain Mapp. 2018;39:4404–4419.
Xue K, Liang S, Yang B, et al. Local dynamic spontaneous brain activity changes in first‐episode, treatment‐naïve patients with major depressive disorder and their associated gene expression profiles. Psychol Med. 2022;52:2052–2061.
Sun F, Liu Z, Yang J, et al. Shared and distinct patterns of dynamical degree centrality in bipolar disorder across different mood states. Front Psychiatry. 2022;13:941073.
Wang Y, Jiang Y, Su W, et al. Temporal dynamics in degree centrality of brain functional connectome in first‐episode schizophrenia with different short‐term treatment responses: a longitudinal study. Neuropsychiatr Dis Treat. 2021;17:1505–1516. Available from: https://pubmed.ncbi.nlm.nih.gov/34079256/. Accessed 18 May 2021.
Ge J, Peng G, Lyu B, et al. Cross‐language differences in the brain network subserving intelligible speech. Proc Natl Acad Sci USA. 2015;112:2972–2977.
Li Y, Tang C, Lu J, et al. Human cortical encoding of pitch in tonal and non‐tonal languages. Nat Commun. 2021;12:1161.
Huang MZ, Yoon YS, Yang J, et al. In‐bed sensorimotor rehabilitation in early and late subacute stroke using a wearable elbow robot: a pilot study. Front Hum Neurosci. 2021;15:669059.
Zeng J, Liu M, Cui L. Diagnostic criteria of cerebrovascular diseases in China (version 2019). Chin J Neurol. 2019;52:710–715.
Li S, Xiao L, Tian H, et al. Introduction to Chinese standard aphasia examination. Chin J Rehabil Theory Practice. 2000;6:162–164.
XI Y, Yang J, Rena A, et al. The standardization of a Uighur Aphasia battery. Chin J Phys Med Rehabil. 2015;12:509–512.
Yan CG, Wang XD, Zuo XN, et al. DPABI: data processing & analysis for (resting‐state) brain imaging. Neuroinformatics. 2016;14:339–351.
Bandettini PA, Jesmanowicz A, Van Kylen J, et al. Functional MRI of brain activation induced by scanner acoustic noise. Magn Reson Med. 1998;39:410–416.
Nguyen M, Ngo GH, Chen NF. Hierarchical character embeddings: learning phonological and semantic representations in languages of logographic origin using recursive neural networks. IEEE/ACM Trans Audio Speech Lang Process. 2019;28:461–473.
XI Y, ZU F, Liu P, et al. A study of linguistic characteristics and locations of brain lesions in Uyghur and Chinese aphasia caused by stroke. Chin J Phys Med Rehabil. 2011;12:819–822.
Belger A, Puce A, Krystal JH, et al. Dissociation of mnemonic and perceptual processes during spatial and nonspatial working memory using fMRI. Hum Brain Mapp. 1998;6:14–32.
O'Brien BA, Habib Mohamed MB, Arshad NA, et al. The impact of different writing systems on children's spelling error profiles: alphabetic, Akshara, and Hanzi cases. Front Psychol. 2020;11:870.
Xu M, Wang T, Chen S, et al. Effective connectivity of brain regions related to visual word recognition: an fMRI study of Chinese reading. Hum Brain Mapp. 2015;36:2580–2591.
Han L, Ke J, Zhang D, et al. Altered functional connectivity in language and non‐language brain networks in patients diagnosed with acute post‐stroke aphasia. Clin Neurol Neurosurg. 2023;235:108044.
Li H, Zhang H, Xu S, et al. Altered spontaneous brain activity in poststroke aphasia: a resting‐state fMRI study. Brain Sci. 2023;13:300.
Liu Y, Perfetti CA. The time course of brain activity in reading English and Chinese: an ERP study of Chinese bilinguals. Hum Brain Mapp. 2003;18:167–175.
Roser ME, Fiser J, Aslin RN, et al. Right hemisphere dominance in visual statistical learning. J Cogn Neurosci. 2011;23:1088–1099.
Schulz L, Ischebeck A, Wriessnegger SC, et al. Action affordances and visuo‐spatial complexity in motor imagery: an fMRI study. Brain Cogn. 2018;124:37–46.
Wenderoth N, Debaere F, Sunaert S, et al. The role of anterior cingulate cortex and precuneus in the coordination of motor behaviour. Eur J Neurosci. 2005;22:235–246.
Hanakawa T, Immisch I, Toma K, et al. Functional properties of brain areas associated with motor execution and imagery. J Neurophysiol. 2003;89:989–1002.
Xing S, Lacey EH, Skipper‐Kallal LM, et al. Right hemisphere grey matter structure and language outcomes in chronic left hemisphere stroke. Brain. 2016;139:227–241.
Geranmayeh F, Brownsett SL, Wise RJ. Task‐induced brain activity in aphasic stroke patients: what is driving recovery? Brain. 2014;137:2632–2648.
Prater S, Anand N, Wei L, Horner N. Crossed aphasia in a patient with anaplastic astrocytoma of the non‐dominant hemisphere. J Radiol Case Rep. 2017;11:1–9.
Osa García A, Brambati SM, Brisebois A, et al. Predicting early post‐stroke aphasia outcome from initial aphasia severity. Front Neurol. 2020;11:120.