ArticlePublisher preview availableLiterature Review

The role of language-related functional brain regions and white matter tracts in network plasticity of post-stroke aphasia

April 2024
Journal of Neurology 271(6):1-21

April 2024
271(6):1-21

Authors:

The neural mechanisms underlying language recovery after a stroke remain controversial. This review aimed to summarize the plasticity and reorganization mechanisms of the language network through neuroimaging studies. Initially, we discussed the involvement of right language homologues, perilesional tissue, and domain-general networks. Subsequently, we summarized the white matter functional mapping and remodeling mechanisms associated with language subskills. Finally, we explored how non-invasive brain stimulation (NIBS) promoted language recovery by inducing neural network plasticity. It was observed that the recruitment of right hemisphere language area homologues played a pivotal role in the early stages of frontal post-stroke aphasia (PSA), particularly in patients with larger lesions. Perilesional plasticity correlated with improved speech performance and prognosis. The domain-general networks could respond to increased “effort” in a task-dependent manner from the top-down when the downstream language network was impaired. Fluency, repetition, comprehension, naming, and reading skills exhibited overlapping and unique dual-pathway functional mapping models. In the acute phase, the structural remodeling of white matter tracts became challenging, with recovery predominantly dependent on cortical activation. Similar to the pattern of cortical activation, during the subacute and chronic phases, improvements in language functions depended, respectively, on the remodeling of right white matter tracts and the restoration of left-lateralized language structural network patterns. Moreover, the midline superior frontal gyrus/dorsal anterior cingulate cortex emerged as a promising target for NIBS. These findings offered theoretical insights for the early personalized treatment of aphasia after stroke.

Cortex-related compensation mechanisms of PSA in different periods. In the acute phases, activation of perilesional tissue is associated with good speech performance and prognosis. In the subacute phases, the activation of domain-general networks, especially bilateral DLPFC, bilateral preSMA/dACC, and left precuneus involved in the general cognitive control process, might compensate for specific impaired language functions in a task-dependent manner from the top-down. The recruitment of right homologue language areas also partially compensates for language deficits. In the chronic phase, good long-term language outcomes largely depend on the preservation and restoration of near-normal function in the left language areas. PSA: post-stroke aphasia, DLPFC: dorsolateral prefrontal cortex, SMA: supplementary motor area, dACC: dorsal anterior cingulate cortex

…

Language-related dual-stream models and function mapping. The dorsal stream is composed of the AF and SLF, connecting the posterosuperior temporal with inferior frontal cortices and mapping sound to articulation. The ventral stream consists of the MdLF, ILF, IFOF, and UF, connecting the temporal-pole to the basal occipitotemporal cortex and mapping sound to meaning. FAT connects the SMA with the IFG and is critical for speech initiation and fluency. Corpus callosum fibers connecting the left SMA, Broca’s area, and Wernicke’s area with right homologous regions also plays a key role in fluency and reading. SMA: supplementary motor area, SMG: supramarginal gyrus, AG: angular gyrus, FAT: frontal aslant tract, SLF: superior longitudinal fasciculus, AF: arcuate fasciculus, MdLF: middle longitudinal fasciculus, IFOF: inferior fronto-occipital fasciculus, ILF: inferior longitudinal fasciculus, UF: uncinate fasciculus. ○: cortex, □: fiber

…

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Vol.:(0123456789)

Journal of Neurology (2024) 271:3095–3115

https://doi.org/10.1007/s00415-024-12358-5

REVIEW

The role oflanguage‑related functional brain regions andwhite

matter tracts innetwork plasticity ofpost‑stroke aphasia

YueHan1· YuanyuanJing1· YanminShi2· HongbinMo1· YafeiWan1· HongweiZhou3· FangDeng1

Received: 5 January 2024 / Revised: 26 March 2024 / Accepted: 27 March 2024 / Published online: 12 April 2024

Abstract

The neural mechanisms underlying language recovery after a stroke remain controversial. This review aimed to summarize

the plasticity and reorganization mechanisms of the language network through neuroimaging studies. Initially, we discussed

the involvement of right language homologues, perilesional tissue, and domain-general networks. Subsequently, we sum-

marized the white matter functional mapping and remodeling mechanisms associated with language subskills. Finally, we

explored how non-invasive brain stimulation (NIBS) promoted language recovery by inducing neural network plasticity. It

was observed that the recruitment of right hemisphere language area homologues played a pivotal role in the early stages of

frontal post-stroke aphasia (PSA), particularly in patients with larger lesions. Perilesional plasticity correlated with improved

speech performance and prognosis. The domain-general networks could respond to increased “eﬀort” in a task-dependent

manner from the top-down when the downstream language network was impaired. Fluency, repetition, comprehension,

naming, and reading skills exhibited overlapping and unique dual-pathway functional mapping models. In the acute phase,

the structural remodeling of white matter tracts became challenging, with recovery predominantly dependent on cortical

activation. Similar to the pattern of cortical activation, during the subacute and chronic phases, improvements in language

functions depended, respectively, on the remodeling of right white matter tracts and the restoration of left-lateralized language

structural network patterns. Moreover, the midline superior frontal gyrus/dorsal anterior cingulate cortex emerged as a prom-

ising target for NIBS. These ﬁndings oﬀered theoretical insights for the early personalized treatment of aphasia after stroke.

Keywords Stroke· Aphasia· Plasticity· Brain regions· White matter· Non-invasive brain stimulation

Introduction

Left middle cerebral artery stroke often results in damage to

the language network, leading to aphasia [1]. It is estimated

that more than 10 million new stroke cases are reported each

year globally, with at least one-third of patients experiencing

aphasia symptoms [1–3]. Post-stroke aphasia (PSA) refers to

the acquired language disorder caused by stroke destroying

the language functional areas of the dominant hemisphere. It

is characterized by varying degrees of impairment in sponta-

neous speech, auditory comprehension, repetition, naming,

reading, and writing abilities [4]. Aphasia is one of the most

* Hongwei Zhou

hwzhou@jlu.edu.cn

* Fang Deng

deng_fang@jlu.edu.cn

Yue Han

2661453367@qq.com

Yuanyuan Jing

jsl1532857149@163.com

Yanmin Shi

1299459741@qq.com

Hongbin Mo

m15590315039@163.com

Yafei Wan

wanyafei_e@163.com

1 Department ofNeurology, The First Hospital ofJilin

University, Changchun, China

2 Health Management (Physical Examination) Center, The

Second Norman Bethune Hospital ofJilin University,

Changchun, China

3 Department ofRadiology, The First Hospital ofJilin

University, Changchun, China

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The role of language-related functional brain regions and white matter tracts in network plasticity of post-stroke aphasia

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