Differential reorganization of three syntax-related networks induced by a left frontal glioma

Ryuta Kinno, Shinri Ohta, Yoshihiro Muragaki, Takashi Maruyama, Kuniyoshi L. Sakai

Research output: Contribution to journalArticle

27 Citations (Scopus)

Abstract

The opercular/triangular parts of the left inferior frontal gyrus and the left lateral premotor cortex are critical in syntactic processing. We have recently indicated that a glioma in one of these regions is sufficient to cause agrammatic comprehension. In the present study, we aimed to show how normally existing syntax-related networks are functionally reorganized by a lesion. Twenty-one patients with a left frontal glioma preoperatively performed a picture-sentence matching task, and underwent functional magnetic resonance imaging scans in an event-related design. We established two qualitatively different types of agrammatic comprehension, depending on glioma location. Patients with a glioma in the left lateral premotor cortex had a more profound deficit in the comprehension of scrambled sentences than that of active and passive sentences. In contrast, patients with a glioma in the opercular/triangular parts of the left inferior frontal gyrus had a more profound deficit in the comprehension of passive and scrambled sentences than that of active sentences. Moreover, we found dramatic changes in the activation patterns in these two patient groups, which accompanied abnormal overactivity and/or underactivity in the syntax-related regions. Furthermore, by examining functional connectivity in the normal brain, we identified three syntax-related networks among those regions, and anatomically visualized connections within individual networks by using diffusion tensor imaging. The first network consists of the opercular/triangular parts of the left inferior frontal gyrus, left intraparietal sulcus, right frontal regions, presupplementary motor area, and right temporal regions. These regions were overactivated in the patients with a glioma in the left lateral premotor cortex only for correct responses, indicating a cognitive change. The second network consists of the left lateral premotor cortex, left angular gyrus, lingual gyrus, and cerebellar nuclei. These regions were overactivated in the patients with a glioma in the opercular/triangular parts of the left inferior frontal gyrus for both correct and incorrect responses, indicating a neuronal change. The third network consists of the left ventral frontal and posterior temporal regions. These regions were underactivated in the patients with a glioma in the opercular/triangular parts of the left inferior frontal gyrus, indicating another neuronal change. These results demonstrate that agrammatic comprehension is associated with the global reorganization of functionally distinct networks, which indeed reflects a differential change in the relative contribution of these three networks to normal syntax-related functions.

Original languageEnglish
Pages (from-to)1193-1212
Number of pages20
JournalBrain
Volume137
Issue number4
DOIs
Publication statusPublished - Jan 1 2014
Externally publishedYes

Fingerprint

Glioma
Motor Cortex
Prefrontal Cortex
Parietal Lobe
Temporal Lobe
Cerebellar Nuclei
Occipital Lobe
Diffusion Tensor Imaging
Magnetic Resonance Imaging
Brain

All Science Journal Classification (ASJC) codes

  • Clinical Neurology

Cite this

Differential reorganization of three syntax-related networks induced by a left frontal glioma. / Kinno, Ryuta; Ohta, Shinri; Muragaki, Yoshihiro; Maruyama, Takashi; Sakai, Kuniyoshi L.

In: Brain, Vol. 137, No. 4, 01.01.2014, p. 1193-1212.

Research output: Contribution to journalArticle

Kinno, Ryuta ; Ohta, Shinri ; Muragaki, Yoshihiro ; Maruyama, Takashi ; Sakai, Kuniyoshi L. / Differential reorganization of three syntax-related networks induced by a left frontal glioma. In: Brain. 2014 ; Vol. 137, No. 4. pp. 1193-1212.
@article{df586b113c554a90810750ebc96e58d1,
title = "Differential reorganization of three syntax-related networks induced by a left frontal glioma",
abstract = "The opercular/triangular parts of the left inferior frontal gyrus and the left lateral premotor cortex are critical in syntactic processing. We have recently indicated that a glioma in one of these regions is sufficient to cause agrammatic comprehension. In the present study, we aimed to show how normally existing syntax-related networks are functionally reorganized by a lesion. Twenty-one patients with a left frontal glioma preoperatively performed a picture-sentence matching task, and underwent functional magnetic resonance imaging scans in an event-related design. We established two qualitatively different types of agrammatic comprehension, depending on glioma location. Patients with a glioma in the left lateral premotor cortex had a more profound deficit in the comprehension of scrambled sentences than that of active and passive sentences. In contrast, patients with a glioma in the opercular/triangular parts of the left inferior frontal gyrus had a more profound deficit in the comprehension of passive and scrambled sentences than that of active sentences. Moreover, we found dramatic changes in the activation patterns in these two patient groups, which accompanied abnormal overactivity and/or underactivity in the syntax-related regions. Furthermore, by examining functional connectivity in the normal brain, we identified three syntax-related networks among those regions, and anatomically visualized connections within individual networks by using diffusion tensor imaging. The first network consists of the opercular/triangular parts of the left inferior frontal gyrus, left intraparietal sulcus, right frontal regions, presupplementary motor area, and right temporal regions. These regions were overactivated in the patients with a glioma in the left lateral premotor cortex only for correct responses, indicating a cognitive change. The second network consists of the left lateral premotor cortex, left angular gyrus, lingual gyrus, and cerebellar nuclei. These regions were overactivated in the patients with a glioma in the opercular/triangular parts of the left inferior frontal gyrus for both correct and incorrect responses, indicating a neuronal change. The third network consists of the left ventral frontal and posterior temporal regions. These regions were underactivated in the patients with a glioma in the opercular/triangular parts of the left inferior frontal gyrus, indicating another neuronal change. These results demonstrate that agrammatic comprehension is associated with the global reorganization of functionally distinct networks, which indeed reflects a differential change in the relative contribution of these three networks to normal syntax-related functions.",
author = "Ryuta Kinno and Shinri Ohta and Yoshihiro Muragaki and Takashi Maruyama and Sakai, {Kuniyoshi L.}",
year = "2014",
month = "1",
day = "1",
doi = "10.1093/brain/awu013",
language = "English",
volume = "137",
pages = "1193--1212",
journal = "Brain",
issn = "0006-8950",
publisher = "Oxford University Press",
number = "4",

}

TY - JOUR

T1 - Differential reorganization of three syntax-related networks induced by a left frontal glioma

AU - Kinno, Ryuta

AU - Ohta, Shinri

AU - Muragaki, Yoshihiro

AU - Maruyama, Takashi

AU - Sakai, Kuniyoshi L.

PY - 2014/1/1

Y1 - 2014/1/1

N2 - The opercular/triangular parts of the left inferior frontal gyrus and the left lateral premotor cortex are critical in syntactic processing. We have recently indicated that a glioma in one of these regions is sufficient to cause agrammatic comprehension. In the present study, we aimed to show how normally existing syntax-related networks are functionally reorganized by a lesion. Twenty-one patients with a left frontal glioma preoperatively performed a picture-sentence matching task, and underwent functional magnetic resonance imaging scans in an event-related design. We established two qualitatively different types of agrammatic comprehension, depending on glioma location. Patients with a glioma in the left lateral premotor cortex had a more profound deficit in the comprehension of scrambled sentences than that of active and passive sentences. In contrast, patients with a glioma in the opercular/triangular parts of the left inferior frontal gyrus had a more profound deficit in the comprehension of passive and scrambled sentences than that of active sentences. Moreover, we found dramatic changes in the activation patterns in these two patient groups, which accompanied abnormal overactivity and/or underactivity in the syntax-related regions. Furthermore, by examining functional connectivity in the normal brain, we identified three syntax-related networks among those regions, and anatomically visualized connections within individual networks by using diffusion tensor imaging. The first network consists of the opercular/triangular parts of the left inferior frontal gyrus, left intraparietal sulcus, right frontal regions, presupplementary motor area, and right temporal regions. These regions were overactivated in the patients with a glioma in the left lateral premotor cortex only for correct responses, indicating a cognitive change. The second network consists of the left lateral premotor cortex, left angular gyrus, lingual gyrus, and cerebellar nuclei. These regions were overactivated in the patients with a glioma in the opercular/triangular parts of the left inferior frontal gyrus for both correct and incorrect responses, indicating a neuronal change. The third network consists of the left ventral frontal and posterior temporal regions. These regions were underactivated in the patients with a glioma in the opercular/triangular parts of the left inferior frontal gyrus, indicating another neuronal change. These results demonstrate that agrammatic comprehension is associated with the global reorganization of functionally distinct networks, which indeed reflects a differential change in the relative contribution of these three networks to normal syntax-related functions.

AB - The opercular/triangular parts of the left inferior frontal gyrus and the left lateral premotor cortex are critical in syntactic processing. We have recently indicated that a glioma in one of these regions is sufficient to cause agrammatic comprehension. In the present study, we aimed to show how normally existing syntax-related networks are functionally reorganized by a lesion. Twenty-one patients with a left frontal glioma preoperatively performed a picture-sentence matching task, and underwent functional magnetic resonance imaging scans in an event-related design. We established two qualitatively different types of agrammatic comprehension, depending on glioma location. Patients with a glioma in the left lateral premotor cortex had a more profound deficit in the comprehension of scrambled sentences than that of active and passive sentences. In contrast, patients with a glioma in the opercular/triangular parts of the left inferior frontal gyrus had a more profound deficit in the comprehension of passive and scrambled sentences than that of active sentences. Moreover, we found dramatic changes in the activation patterns in these two patient groups, which accompanied abnormal overactivity and/or underactivity in the syntax-related regions. Furthermore, by examining functional connectivity in the normal brain, we identified three syntax-related networks among those regions, and anatomically visualized connections within individual networks by using diffusion tensor imaging. The first network consists of the opercular/triangular parts of the left inferior frontal gyrus, left intraparietal sulcus, right frontal regions, presupplementary motor area, and right temporal regions. These regions were overactivated in the patients with a glioma in the left lateral premotor cortex only for correct responses, indicating a cognitive change. The second network consists of the left lateral premotor cortex, left angular gyrus, lingual gyrus, and cerebellar nuclei. These regions were overactivated in the patients with a glioma in the opercular/triangular parts of the left inferior frontal gyrus for both correct and incorrect responses, indicating a neuronal change. The third network consists of the left ventral frontal and posterior temporal regions. These regions were underactivated in the patients with a glioma in the opercular/triangular parts of the left inferior frontal gyrus, indicating another neuronal change. These results demonstrate that agrammatic comprehension is associated with the global reorganization of functionally distinct networks, which indeed reflects a differential change in the relative contribution of these three networks to normal syntax-related functions.

UR - http://www.scopus.com/inward/record.url?scp=84897897620&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84897897620&partnerID=8YFLogxK

U2 - 10.1093/brain/awu013

DO - 10.1093/brain/awu013

M3 - Article

VL - 137

SP - 1193

EP - 1212

JO - Brain

JF - Brain

SN - 0006-8950

IS - 4

ER -