Converging evidence for a cortico-subcortical network mediating lexical retrieval

Abstract

See Hope and Price (doi:10.1093/aww240) for a scientific commentary on this article. Neurological insults that damage the left hemisphere are frequently associated with a variety of language disorders. Of these, lexical retrieval impairments are the most commonly observed, and often constitute the residual but lasting disturbance in patients with good functional outcomes. The current study was specifically designed to understand the anatomical factors that prevent full recovery of lexical retrieval in patients having undergone a neurosurgery for a left diffuse low-grade glioma, with a special focus on white matter disconnection. One hundred and ten patients operated on under local anaesthesia with intraoperative language mapping were included in this study. All benefited from an examination of language in the chronic phase using a picture-naming task. We derived from this task two well-controlled regressed measures of lexical retrieval based on the number of anomic responses and response times. We mapped the resection cavities and the postoperative residual lesion infiltrations (mainly located along the white matter tracts), and used a combination of voxelwise and tractwise lesion-deficit analyses to process the data. All results were corrected for multiple comparisons. For the purpose of comparison, 105 neurologically healthy control participants were further enrolled. At the cortical level, lexical retrieval impairments were mainly associated with resection of the mid-to-posterior part of the left inferior temporal gyrus, as revealed by standard voxel-based lesion-symptom analyses. Multilevel tractwise analyses, including correlations, ridge multiple regressions and group analyses, showed a strong involvement of the left inferior longitudinal fasciculus and, to a lesser extent, of the posterior superior longitudinal fasciculus. Further regression analyses indicated that lasting lexical retrieval impairments were better predicted by considering together both resection-related volume loss in the posterior inferior temporal gyrus and postoperative residual lesion volume in the left inferior longitudinal fasciculus. We conclude that the mid-to-posterior inferior temporal cortex and its underlying connections, especially the left inferior longitudinal fasciculus, are critical structures in the lexical retrieval network. Beyond this new insight, our data have important implications for both intraoperative language monitoring and rehabilitation strategies.