Evidence for a critical role of the left inferior parietal lobule and underlying white matter connectivity in proficient text reading

Author:

Boissonneau Sébastien12,Lemaître Anne-Laure34,Herbet Guillaume345,Ng Sam34,Duffau Hugues345,Moritz-Gasser Sylvie345

Affiliation:

1. Department of Neurosurgery, APHM, CHU Timone, Marseille, France;

2. Inserm, INS, Institute of Neurosciences of Systems, Aix Marseille University, Marseille, France;

3. Department of Neurosurgery, Gui de Chauliac Hospital, Montpellier University Medical Center, Montpellier, France;

4. National Institute for Health and Medical Research (INSERM), U1191, Team "Plasticity of Central Nervous System, Stem Cells and Glial Tumors," Institute of Functional Genomics, University of Montpellier, France; and

5. Department of Speech-Language Therapy, Faculty of Medicine, University of Montpellier, France

Abstract

OBJECTIVE Reading proficiency is an important skill for personal and socio-professional daily life. Neurocognitive models underlie a dual-route organization for word reading, in which information is processed by both a dorsal phonological "assembled phonology route" and a ventral lexical-semantic "addressed phonology route." Because proficient reading should not be reduced to the ability to read words one after another, the current study was designed to shed light on the neural bases specifically underpinning text reading and the relative contributions of each route to this skill. METHODS Twenty-two patients with left-sided, diffuse, low-grade glioma who underwent operations while awake were included. They were divided into 3 groups on the basis of tumor location: the inferior parietal lobule (IPL) group (n = 6), inferior temporal gyrus (Tinf) group (n = 6), and fronto-insular (control) group (n = 10). Spoken language and reading abilities were tested in all patients the day before surgery, during surgery, and 3 months after surgery, and cognitive functioning was evaluated before and 3 months after surgery. Text-reading scores obtained before and 3 months after surgery were compared within each group and between groups, correlations between reading scores and both spoken language and cognitive scores were calculated, postoperative cortical-subcortical resection location was estimated, and multiple regression analysis was conducted to examine the relationship between reading proficiency and lesion location. RESULTS The results indicated that only the patients in the IPL group showed a significant decrease in text-reading scores between periods, which was not associated with lower scores in naming or verbal fluency; patients in the Tinf group showed a slight nonsignificant decrease in text reading between periods, which was associated with a clear decrease in naming and semantic verbal fluency; and patients in the control group showed no differences between preoperative and postoperative reading and spoken language scores. The results of the analysis of these behavioral results and anatomical data (resection cavities and white matter damage) suggest critical roles for the left inferior parietal lobule and underlying white matter connectivity, especially the posterior segment of the arcuate fasciculus, in proficient text reading. CONCLUSIONS Text-reading proficiency may depend on not only the integrity of both processing routes but also their capacity for interaction, with critical roles for the left inferior parietal lobule and posterior arcuate fasciculus. These findings have fundamental as well as clinical implications.

Publisher

Journal of Neurosurgery Publishing Group (JNSPG)

Subject

Genetics,Animal Science and Zoology

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