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.

Dissociating Effects of Scrambling and Topicalization within the Left Frontal and Temporal Language Areas: An fMRI Study in Kaqchikel Maya

“…In recent studies using a visual sentence-picture matching task similar to that used here, we tested 21 patients with a left frontal glioma and observed abnormal overactivity and/or underactivity in 14 syntax-related regions (Kinno et al, 2014, 2015). Those investigations also revealed three syntax-related networks: network I (syntax and its supportive system), network II (syntax and input/output interface), and network III (syntax and semantics).…”

“…Based on our earlier investigations (Kinno et al, 2008, 2014), we used here a modified sentence-picture matching task, in which each participant listened to a Kaqchikel sentence and judged whether a picture matched the meaning of the sentence ( Figure 2 ). The advantage of applying this experimental paradigm to an understudied language such as Kaqchikel is that it will allow us to validate the universality of linguistic computation in the brain.…”

Neural Mechanisms Underlying the Computation of Hierarchical Tree Structures in Mathematics

“…Using a visual picture-sentence matching task, we have recently tested twenty-one patients with a left frontal glioma, and found abnormal overactivity and/or underactivity in 14 syntax-related regions [58]. By examining the functional and anatomical connectivity among those regions, we have clarified three syntax-related networks.…”

Reduced Diffusion Tensor Fractional Anisotropy in the Left Arcuate Fasciculus of Patients with Aphasia Caused by Acute Cerebral Infarct

“…In addition to the arcuate fasciculus and the superior longitudinal fasciculus, recent studies have implicated the uncinate fasciculus and the inferior longitudinal fasciculus in language function. 40,41) Moreover, a recent case report found that a patient with severe damage to the left arcuate fasciculus exhibited good recovery from aphasia. 42) Accordingly, the contribution of the arcuate fasciculus to language function should be interpreted in the context of a wider neural network including the aforementioned structures.…”