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AJNR Awards, New Junior Editors, and more. Read the latest AJNR updates

Research ArticleBRAIN TUMOR IMAGING

Cognitive Control Network and Language Reorganization in Patients with Brain Tumors

Luca Pasquini, Antonio Napolitano, Leonardo Spitoni, Maurizio Schmid, Francesco Dellepiane, Mehrnaz Jenabi, Kyung Peck and Andrei Holodny
American Journal of Neuroradiology May 2025, DOI: https://doi.org/10.3174/ajnr.A8638
Luca Pasquini
aFrom the Neuroradiology Service (L.P.), Radiology Department, Yale New Haven Hospital, Yale Medical School, New Haven, Connecticut
bNeuroradiology Service (L.P., M.J., A.H.), Radiology Department, Memorial Sloan Kettering Cancer Center, New York, New York
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Antonio Napolitano
cMedical Physics Department (A.N., L.S.), Bambino Gesù Children’s Hospital, Rome, Italy
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Leonardo Spitoni
cMedical Physics Department (A.N., L.S.), Bambino Gesù Children’s Hospital, Rome, Italy
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Maurizio Schmid
dDepartment of Engineering (M.S.), University Roma Tre, Rome, Italy
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Francesco Dellepiane
eNeuroradiology Service (F.D.), Radiology Department, Bambino Gesù Children’s Hospital, Rome, Italy
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Mehrnaz Jenabi
bNeuroradiology Service (L.P., M.J., A.H.), Radiology Department, Memorial Sloan Kettering Cancer Center, New York, New York
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Kyung Peck
fDepartment of Medical Physics (K.P.), Memorial Sloan Kettering Cancer Center, New York, New York
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Andrei Holodny
bNeuroradiology Service (L.P., M.J., A.H.), Radiology Department, Memorial Sloan Kettering Cancer Center, New York, New York
gDepartment of Radiology (A.H.), Weill Medical College of Cornell University, New York, New York
hBrain Tumor Center (A.H.), Memorial Sloan Kettering Cancer Center, New York, New York
iDepartment of Neuroscience (A.H.), Weill Cornell Graduate School of the Medical Sciences, New York, New York
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Abstract

BACKGROUND AND PURPOSE: The interaction between language and other cognitive networks in patients harboring brain tumors is poorly understood. We studied the modification of the cognitive control network (CCN) induced by brain tumors and its participation in language reorganization. We hypothesized that patients with brain tumors and reorganized language would show a modification of the CCN compared with patients who remain left dominant.

MATERIALS AND METHODS: Patients were selected with the criteria: newly diagnosed, pathologically-confirmed left-hemispheric tumor; single lesions; right-handedness; task-based and resting-state fMRI; no artifacts. Age-matched healthy controls (HC) were recruited from open-source databases. Language laterality was calculated by using task-based fMRI. We obtained the CCN through ad hoc independent component analysis on resting-state fMRI. Differences in CCN between patients and HC were characterized by cosine similarity (CS) and earth mover’s distance (EMD). Changes related to language reorganization and patients’ speech were assessed with the t test (P < .05). Results were corrected for multiple comparisons.

RESULTS: One hundred forty-two right-handed patients (35 low-grade and 88 high-grade gliomas; 19 metastases) and 184 HC were included. Two independent components of the CCN were obtained. The t test confirmed significant effects of lateralization on the CCN (P = .004). Modification of CCN was associated with fewer speech deficits 1 week after surgery (P = .005).

CONCLUSIONS: This study provides evidence that modifications of CCN occur in the setting of language reorganization. Patients exhibiting these modifications perform better at speech evaluation after surgery, suggesting a role of cognitive control in compensating for speech deficits when language reorganizes.

ABBREVIATIONS:

AAL
automated anatomic labeling
AD
atypical dominant
CCN
cognitive control network
CS
cosine similarity
EMD
earth mover’s distance
FSL
FMRIB Software Library
G-ICA
Group ICA
GIFT
Group ICA of the fMRI Toolbox
GIG-ICA
group-information guided ICA
HC
healthy control
HGG
high-grade glioma
IC
independent component
LD
left dominant
LGG
low-grade glioma
LI
laterality index
MNI
Montreal Neurological Institute
NVU
neuro-vascular uncoupling
RSN
resting-state network

Footnotes

  • Disclosure forms provided by the authors are available with the full text and PDF of this article at www.ajnr.org.

  • This research has been supported by funding from the National Institutes of Health (NIH): grants NIH-NIBIB R01 EB022720 (Holodny, PI), NIH-NCI R21 CA220144 (Holodny and Peck, PIs), NIH-NCI P30 CA008748 (Vickers, PI).

  • © 2025 by American Journal of Neuroradiology
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Cite this article
Luca Pasquini, Antonio Napolitano, Leonardo Spitoni, Maurizio Schmid, Francesco Dellepiane, Mehrnaz Jenabi, Kyung Peck, Andrei Holodny
Cognitive Control Network and Language Reorganization in Patients with Brain Tumors
American Journal of Neuroradiology May 2025, DOI: 10.3174/ajnr.A8638

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Cognitive Control in Tumor Language Plasticity
Luca Pasquini, Antonio Napolitano, Leonardo Spitoni, Maurizio Schmid, Francesco Dellepiane, Mehrnaz Jenabi, Kyung Peck, Andrei Holodny
American Journal of Neuroradiology May 2025, DOI: 10.3174/ajnr.A8638
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