The central role of the left inferior longitudinal fasciculus in the face-name retrieval network

Abstract

Unsuccessful retrieval of proper names (PNs) is commonly observed in patients suffering from neurological conditions such as stroke or epilepsy. While a large body of works has suggested that PN retrieval relies on a cortical network centered on the left anterior temporal lobe (ATL), much less is known about the white matter connections underpinning this process. Sparse studies provided evidence for a possible role of the uncinate fasciculus, but the inferior longitudinal fasciculus (ILF) might also contribute, since it mainly projects into the ATL, interconnects it with the posterior lexical interface and is engaged in common name (CN) retrieval. To ascertain this hypothesis, we assessed 58 patients having undergone a neurosurgery for a left low-grade glioma by means of a famous face naming (FFN) task. The behavioural data were processed following a multilevel lesion approach, including location-based analyses, voxel-based lesion-symptom mapping (VLSM) and disconnection-symptom mapping. Different statistical models were generated to control for sociodemographic data, familiarity, biographical knowledge and control cognitive performances (i.e., semantic and episodic memory and CN retrieval). Overall, VLSM analyses indicated that damage to the mid-to-anterior part of the ventro-basal temporal cortex was especially associated with PN retrieval deficits. As expected, tract-oriented analyses showed that the left ILF was the most strongly associated pathway. Our results provide evidence for the pivotal role of the ILF in the PN retrieval network. This novel finding paves the way for a better understanding of the pathophysiological bases underlying PN retrieval difficulties in the various neurological conditions marked by white matter abnormalities.

Keywords: inferior longitudinal fasciculus; lower-grade glioma; proper name retrieval; structural disconnection; temporal lobe.

FIGURE 1

Overlap map of resection cavities for all patients. The colour code indicates the number of lesions at each voxel. The maximum overlap occurred in the temporal pole. ITG, inferior temporal gyrus; dmPFC, dorso‐medial prefrontal cortex.

FIGURE 2

Anatomical data by group. (a) Lesion overlap map for each patient subgroup. (b) Disconnection data for both the inferior longitudinal and the uncinate fasciculi. dmPFC, dorso‐medial prefrontal cortex; ILF, inferior longitudinal fasciculus; UF, uncinate fasciculus; TP, temporal pole; mpITG, mid‐to‐posterior inferior temporal gyrus; F, frontal; FTI, fronto‐temporo‐insular; T, temporal; TTP, temporal including temporal pole.

FIGURE 3

Combined violin and box plot of behavioural data for (a) all patients versus control participants, (b) the three patient subgroups and (c) the four patient subgroups. For each boxplot, the horizontal line at the center indicates the median value, the lower and upper bounds of the box 25–75% interquartile range and whiskers indicate 1.5× interquartile range. The central white dots indicate mean and the white bars indicate standard deviations. All individual data are plotted. Statistical results are fully described in the main text.

FIGURE 4

VLSM results. For each regression model, the permutation‐derived p‐map is plotted onto a 3D rendering with a threshold of p < .005 at the peak level and p < .05 at the cluster level. An ordered polar barplot indicates the percentage of significant voxels for each AAL parcel covered by significant voxels in a proportion of at least 5%. TP, temporal pole; ITG, inferior temporal gyrus; ParaH, para‐hippocampal gyrus; Fusi, fusiform gyrus; MTG, middle temporal gyrus; Hippo, hippocampus; Amg, amygdala.

FIGURE 5

Results from disconnection analyses. Tracts are ordered as a function of the length of the Spearman correlation. Significant tracts are coloured in pink in the four subfigures. AC, anterior commissure; AF, arcuate fasciculus; CC_Midant, corpus callosum in its mid‐anterior part; CC_post, corpus callosum in its posterior part; Cing_FP, cingulum frontal parietal; Cing_ParaH, cingulum para‐hippocampal; Cing_PhippP, cingulum para‐hippocampal parietal; CPT_F, cortico‐pontine tract frontal; CST_ant, cortico‐striatal tract anterior; CST_sup, cortico‐striatal tract superior; EmC, extreme capsule; FAT, frontal aslant tract; IFOF, inferior fronto‐occipital fasciculus; ILF, inferior longitudinal fasciculus; RST, reticulo‐spinal tract; SLF_I, superior longitudinal fasciculus (branch I); SLF_II, superior longitudinal fasciculus (branch II); Th_ant, thalamic radiation anterior; Th_sup, thalamic radiation superior; UF, uncinate fasciculus.

FIGURE 6

Spatial correlation results for each model. Bars indicate the t scores. For models 1 and 2, only suprathresholded voxels after FWE correction are displayed. For models 3 and 4, a lenient threshold of p < .0001 uncorrected is used (see main text). In each model, significant voxels overlap with the known spatial positioning of the left ILF.

FIGURE 7

Neuroanatomical data of single cases. The resection cavities of patient C.G. (left‐hander, upper part) and patient A.S. (right‐hander, lower part) are plotted onto a three‐dimensional MNI152 rendering (left). The related disconnection maps (right) are displayed on descending sagittal slides. The colour code indicates the disconnection probability at each voxel.